In Vivo Single-Cell Detection of Metabolic Oscillations in Stem Cells

Cell Reports

Volumn 10, Issue 1, 2015, Pages 1-7

  Stringari, Chiara ^a,b   Wang, Hong ^c,d   Geyfman, Mikhail ^c   Crosignani, Viera ^a   Kumar, Vivek ^e,f   Takahashi, Joseph S ^e,f   Andersen, Bogi ^a,c   Gratton, Enrico ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LABORATOIRE D OPTIQUE ET BIOSCIENCES   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CHINA AGRICULTURAL UNIVERSITY   (China)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; ARNTL PROTEIN, MOUSE; CIRCADIAN RHYTHM SIGNALING PROTEIN; TRANSCRIPTION FACTOR ARNTL;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL CELL; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL HETEROGENEITY; CELL METABOLISM; CELL PROLIFERATION; CELL PROTECTION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DNA SYNTHESIS; EPIDERMAL STEM CELL; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE MICROSCOPY; GENOTOXICITY; GLYCOLYSIS; IMAGE ANALYSIS; IN VIVO STUDY; METABOLIC REGULATION; MICROSCOPY; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; SINGLE CELL ANALYSIS; STEM CELL; TWO PHOTON EXCITATION MICROSCOPY; ANIMAL; CYTOLOGY; DNA DAMAGE; GENETICS; HOMEOSTASIS; HUMAN; METABOLISM;

MUS;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CELL PROLIFERATION; CIRCADIAN CLOCKS; DNA DAMAGE; GLYCOLYSIS; HOMEOSTASIS; HUMANS; MICE; OXIDATIVE PHOSPHORYLATION; PERIOD CIRCADIAN PROTEINS; SINGLE-CELL ANALYSIS; STEM CELLS;

EID: 84920864502     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.12.007     Document Type: Article

References (32)

1. Bass J., Takahashi J.S. Circadian integration of metabolism and energetics. Science 2010, 330:1349-1354.
2. Bird D.K., Yan L., Vrotsos K.M., Eliceiri K.W., Vaughan E.M., Keely P.J., White J.G., Ramanujam N. Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH. Cancer Res. 2005, 65:8766-8773.
3. Bjarnason G.A., Jordan R. Rhythms in human gastrointestinal mucosa and skin. Chronobiol. Int. 2002, 19:129-140.
4. Brown W.R. A review and mathematical analysis of circadian rhythms in cell proliferation in mouse, rat, and human epidermis. J.Invest. Dermatol. 1991, 97:273-280.
5. Bunger M.K., Wilsbacher L.D., Moran S.M., Clendenin C., Radcliffe L.A., Hogenesch J.B., Simon M.C., Takahashi J.S., Bradfield C.A. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 2000, 103:1009-1017.
6. Cheng H., Alvarez-Saavedra M., Dziema H., Choi Y.S., Li A., Obrietan K. Segregation of expression of mPeriod gene homologs in neurons and glia: possible divergent roles of mPeriod1 and mPeriod2 in the brain. Hum. Mol. Genet. 2009, 18:3110-3124.
7. Clayton E., Doupe D.P., Klein A.M., Winton D.J., Simons B.D., Jones P.H. A single type of progenitor cell maintains normal epidermis. Nature 2007, 446:185-189.
8. Colyer R., Lee C., Gratton E. A novel fluorescence lifetime imaging system that optimizes photon efficiency. Microsc. Res. Tech. 2008, 71:201-213.
9. D'Autreaux B., Toledano M.B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 2007, 8:813-824.
10. Digman M., Caiolfa V.R., Zamai M., Gratton E. The phasor approach to fluorescence lifetime imaging analysis. Biophys. J. 2008, 94:L14-L16.
11. Eckel-Mahan K., Sassone-Corsi P. Metabolism and the circadian clock converge. Physiol. Rev. 2013, 93:107-135.
12. Gaddameedhi S., Selby C.P., Kaufmann W.K., Smart R.C., Sancar A. Control of skin cancer by the circadian rhythm. Proc. Natl. Acad. Sci. USA 2011, 108:18790-18795.
13. Geyfman M., Kumar V., Liu Q., Ruiz R., Gordon W., Espitia F., Cam E., Millar S.E., Smyth P., Ihler A., et al. Brain and muscle Arnt-like protein-1 (BMAL1) controls circadian cell proliferation and susceptibility to UVB-induced DNA damage in the epidermis. Proc. Natl. Acad. Sci. USA 2012, 109:11758-11763.
14. Hamanaka R., Chandel N.S. Cell biology. Warburg effect and redox balance. Science 2011, 334:1219-1220.
15. Heikal A.A. Intracellular coenzymes as natural biomarkers for metabolic activities and mitochondrial anomalies. Biomarkers Med. 2010, 4:241-263.
16. Janich P., Pascual G., Merlos-Suarez A., Batlle E., Ripperger J., Albrecht U., Cheng H.Y., Obrietan K., Di Croce L., Benitah S.A. The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 2011, 480:209-214.
17. Janich P., Toufighi K., Solanas G., Luis N.M., Minkwitz S., Serrano L., Lehner B., Benitah S.A. Human epidermal stem cell function is regulated by circadian oscillations. Cell Stem Cell 2013, 13:745-753.
18. Kondratov R.V., Kondratova A.A., Gorbacheva V.Y., Vykhovanets O.V., Antoch M.P. Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev. 2006, 20:1868-1873.
19. Konig K., Riemann I. High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution. J.Biomed. Opt. 2003, 8:432-439.
20. Lim X., Tan S.H., Koh W.L., Chau R.M., Yan K.S., Kuo C.J., van Amerongen R., Klein A.M., Nusse R. Interfollicular epidermal stem cells self-renew via autocrine Wnt signaling. Science 2013, 342:1226-1230.
21. Mascre G., Dekoninck S., Drogat B., Youssef K.K., Brohee S., Sotiropoulou P.A., Simons B.D., Blanpain C. Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 2012, 489:257-262.
22. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
23. Peek C., Affinati A.H., Ramsey K.M., Kuo H.Y., Yu W., Sena L.A., Ilkayeva O., Marcheva B., Kobayashi Y., Omura C., et al. Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 2013, 342:1243417.
24. Plikus M., Vollmers C., de la Cruz D., Chaix A., Ramos R., Panda S., Chuong C.M. Local circadian clock gates cell cycle progression of transient amplifying cells during regenerative hair cycling. Proc. Natl. Acad. Sci. USA 2013, 110:E2106-E2115.
25. Potten C.S., Al-Barwari S.E., Hume W.J., Searle J. Circadian rhythms of presumptive stem cells in three different epithelia of the mouse. Cell Tissue Kinet. 1977, 10:557-568.
26. Sahar S., Sassone-Corsi P. Metabolism and cancer: the circadian clock connection. Nat. Rev. Cancer 2009, 9:886-896.
27. Skala M.C., Riching K.M., Gendron-Fitzpatrick A., Eickhoff J., Eliceiri K.W., White J.G., Ramanujam N. Invivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia. Proc. Natl. Acad. Sci. USA 2007, 104:19494-19499.
28. Stringari C., Cinquin A., Cinquin O., Digman M.A., Donovan P.J., Gratton E. Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue. Proc. Natl. Acad. Sci. USA 2011, 108:13582-13587.
29. Stringari C., Edwards R.A., Pate K.T., Waterman M.L., Donovan P.J., Gratton E. Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH. Sci. Rep. 2012, 2:568.
30. Stringari C., Nourse J.L., Flanagan L., Gratton E. Phasor Fluorescence Lifetime Microscopy of free and protein-bound NADH reveals neural Stem Cell Differentiation Potential. PLoS ONE 2012, 7:e48014.
31. Tu B., Kudlicki A., Rowicka M., McKnight S.L. Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 2005, 310:1152-1158.
32. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.