Quantitative imaging of subcellular metabolism with stable isotopes and multi-isotope imaging mass spectrometry

Seminars in Cell and Developmental Biology

Volumn 24, Issue 8-9, 2013, Pages 661-667

  Steinhauser, Matthew L ^a   Lechene, Claude P ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b National Resource for Imaging Mass Spectrometry   (United States)

Author keywords

Cell division; Human; Keywords: Stable isotope; Metabolism; Quantitative imaging; Stem cell

Indexed keywords

CALCIUM; CALCIUM 42; CALCIUM 43; CALCIUM 44; CARBON 13; COPPER; COPPER 65; DEUTERIUM; IRON; IRON 54; IRON 57; IRON 58; MAGNESIUM; MAGNESIUM 25; MAGNESIUM 26; NITROGEN 15; OXYGEN 17; OXYGEN 18; RADIOISOTOPE; SELENIUM; SELENIUM 74; SELENIUM 76; SELENIUM 77; SELENIUM 78; STABLE ISOTOPE; UNCLASSIFIED DRUG; UNINDEXED DRUG; ZINC; ZINC 66; ZINC 67; ZINC 68;

CELL GRANULE; CELL METABOLISM; CHROMOSOME; HUMAN; IMAGING; INTESTINE CRYPT; MASS SPECTROMETRY; MOLECULAR IMAGING; MULTI ISOTOPE IMAGING MASS SPECTROMETRY; NONHUMAN; NUCLEIC ACID SYNTHESIS; QUANTITATIVE ANALYSIS; QUANTITATIVE STUDY; REVIEW; TRANSMISSION ELECTRON MICROSCOPY;

CELL DIVISION; HUMAN; KEYWORDS: STABLE ISOTOPE; METABOLISM; QUANTITATIVE IMAGING; STEM CELL;

ANIMALS; HUMANS; IMAGING, THREE-DIMENSIONAL; ISOTOPE LABELING; MASS SPECTROMETRY; METABOLISM; NANOTECHNOLOGY; SUBCELLULAR FRACTIONS;

EID: 84887609768     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2013.05.001     Document Type: Review

References (57)

1. Walker B.E., Leblond C.P. Sites of nucleic acid synthesis in the mouse visualized by radioautography after administration of C14-labelled adenine and thymidine. Experimental Cell Research 1958, 14:510-531.
2. Latt S.A. Microfluorometric detection of deoxyribonucleic acid replication in human metaphase chromosomes. Proceedings of the National Academy of Sciences of the United States of America 1973, 70:3395-3399.
3. Littlefield J.W., Gould E.A. The toxic effect of 5-bromodeoxyuridine on cultured epithelial cells. Journal of Biological Chemistry 1960, 235:1129-1133.
4. Matsuoka K., Nomura K., Hoshino T. Mutagenic effects of brief exposure to bromodeoxyuridine on mouse FM3A cells. Cell and Tissue Kinetics 1990, 23:495-503.
5. Lansdorp P.M. Immortal strands? Give me a break. Cell 2007, 129:1244-1247.
6. Rando T.A. The immortal strand hypothesis: segregation and reconstruction. Cell 2007, 129:1239-1243.
7. Cairns J. Mutation selection and the natural history of cancer. Nature 1975, 255:197-200.
8. Lechene C., Hillion F., McMahon G., Benson D., Kleinfeld A.M., Kampf J.P., et al. High-resolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. Journal of Biology 2006, 5:20.
9. Schoenheimer R., Rittenberg D., Foster G.L., Keston A.S., Ratner S. The application of the nitrogen isotope N15 for the study of protein metabolism. Science 1938, 88:599-600.
10. Schoenheimer R., Rittenberg D. The application of isotopes to the study of intermediary metabolism. Science 1938, 87:221-226.
11. Schoenheimer R. The investigation of intermediary metabolism with the aid of heavy hydrogen: Harvey lecture, January 21, 1937. Bulletin of the New York Academy of Medicine 1937, 13:272-295.
12. Schoenheimer R., Rittenberg D. Deuterium as an indicator in the study of intermediary metabolism. Science 1935, 82:156-157.
13. Belanger L.F., Leblond C.P. A method for locating radioactive elements in tissues by covering histological sections with a photographic emulsion. Endocrinology 1946, 39:8-13.
14. Hu V.W., Black G.E., Torres-Duarte A., Abramson F.P. 3H-thymidine is a defective tool with which to measure rates of DNA synthesis. FASEB Journal 2002, 16:1456-1457.
15. Shaner N.C., Steinbach P.A., Tsien R.Y. A guide to choosing fluorescent proteins. Nature Methods 2005, 2:905-909.
16. Liu H.S., Jan M.S., Chou C.K., Chen P.H., Ke N.J. Is green fluorescent protein toxic to the living cells?. Biochemical and Biophysical Research Communications 1999, 260:712-717.
17. Wilson A., Laurenti E., Oser G., van der Wath R.C., Blanco-Bose W., Jaworski M., et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008, 135:1118-1129.
18. Urey H.C. The separation and properties of the isotopes of hydrogen. Science 1933, 78:566-571.
19. Sturup S., Hansen H.R., Gammelgaard B. Application of enriched stable isotopes as tracers in biological systems: a critical review. Analytical and Bioanalytical Chemistry 2008, 390:541-554.
20. Lester W., Sun S.H., Seber A. Observations on the influence of deuterium on bacterial growth. Annals of the NewYork Academy of Sciences 1960, 84:667-677.
21. Lewis G.N. The biology of heavy water. Science 1934, 79:151-153.
22. Barbour H.G. The basis of the pharmacological action of heavy water in mammals. Yale Journal of Biology and Medicine 1937, 9:551-565.
23. Schellekens R.C., Stellaard F., Woerdenbag H.J., Frijlink H.W., Kosterink J.G. Applications of stable isotopes in clinical pharmacology. British Journal of Clinical Pharmacology 2011, 72:879-897.
24. Brand W.A., Coplen T.B. Stable isotope deltas: tiny, yet robust signatures in nature. Isotopes in Environmental and Health Studies 2012.
25. Snider M.J., Reinhardt L., Wolfenden R., Cleland W.W. 15N kinetic isotope effects on uncatalyzed and enzymatic deamination of cytidine. Biochemistry 2002, 41:415-421.
26. Gregg C.T., Hutson J.Y., Prine J.R., Ott D.G., Furchner J.E. Substantial replacement of mammalian body carbon with carbon-13. Life Sciences 1973, 13:775-782.
27. Samuel D., Wof A., Meshorer A., Wasserman I. The effect of 18O on the growth and reproduction of mice. Stable Isotopes: Proceedings of the Third International Conference 1973, 353-360.
28. Koletzko B., Demmelmair H., Hartl W., Kindermann A., Koletzko S., Sauerwald T., et al. The use of stable isotope techniques for nutritional and metabolic research in paediatrics. Early Human Development 1998, 53(Suppl.):S77-S97.
29. Koletzko B., Sauerwald T., Demmelmair H. Safety of stable isotope use. European Journal of Pediatrics 1997, 156(Suppl. 1):S12-S17.
30. Castaing R., Slodzian G.J. Optique corpusculaire-premiers essais de microanalyse par emission ionique secondaire. Microscopie 1962, 1:395-399.
31. Liebl H. Ion microprobe mass analyzer. Journal of Applied Physics 1967, 38:5277-5283.
32. Slodzian G., Daigne B., Girard F., Boust F., Hillion F. Scanning secondary ion analytical microscopy with parallel detection. Biologie Cellulaire 1992, 74:43-50.
33. McMahon G., Saint-Cyr H.F., Lechene C., Unkefer C.J. CN-secondary ions form by recombination as demonstrated using multi-isotope mass spectrometry of 13C- and 15N-labeled polyglycine. Journal of the American Society for Mass Spectrometry 2006, 17:1181-1187.
34. Polerecky L., Adam B., Milucka J., Musat N., Vagner T., Kuypers M.M. Look@NanoSIMS - a tool for the analysis of nanoSIMS data in environmental microbiology. Environmental Microbiology 2012, 14:1009-1023.
35. Gormanns P., Reckow S., Poczatek J.C., Turck C.W., Lechene C. Segmentation of multi-isotope imaging mass spectrometry data for semi-automatic detection of regions of interest. PLoS ONE 2012, 7:e30576.
36. Zhang D.S., Piazza V., Perrin B.J., Rzadzinska A.K., Poczatek J.C., Wang M., et al. Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell stereocilia. Nature 2012, 481:520-524.
37. Peteranderl R., Lechene C. Measure of carbon and nitrogen stable isotope ratios in cultured cells. Journal of the American Society for Mass Spectrometry 2004, 15:478-485.
38. Guerquin-Kern J.L., Hillion F., Madelmont J.C., Labarre P., Papon J., Croisy A. Ultra-structural cell distribution of the melanoma marker iodobenzamide: improved potentiality of SIMS imaging in life sciences. Biomedical Engineering Online 2004, 3:10.
39. Steinhauser M.L., Bailey A.P., Senyo S.E., Guillermier C., Perlstein T.S., Gould A.P., et al. Multi-isotope imaging mass spectrometry quantifies stem cell division and metabolism. Nature 2012, 481:516-519.
40. Hallegot P., Peteranderl R., Lechene C. In-situ imaging mass spectrometry analysis of melanin granules in the human hair shaft. Journal of Investigative Dermatology 2004, 122:381-386.
41. Lechene C.P., Luyten Y., McMahon G., Distel D.L. Quantitative imaging of nitrogen fixation by individual bacteria within animal cells. Science 2007, 317:1563-1566.
42. Popa R., Weber P.K., Pett-Ridge J., Finzi J.A., Fallon S.J., Hutcheon I.D., et al. Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides. ISME Journal 2007, 1:354-360.
43. Dekas A.E., Poretsky R.S., Orphan V.J. Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 2009, 326:422-426.
44. Halm H., Musat N., Lam P., Langlois R., Musat F., Peduzzi S., et al. Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environmental Microbiology 2009, 11:1945-1958.
45. Finzi-Hart J.A., Pett-Ridge J., Weber P.K., Popa R., Fallon S.J., Gunderson T., et al. Fixation and fate of C and N in the cyanobacterium trichodesmium using nanometer-scale secondary ion mass spectrometry. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:6345-6350.
46. Kleinfeld A.M., Kampf J.P., Lechene C. Transport of 13C-oleate in adipocytes measured using multi imaging mass spectrometry. Journal of the American Society for Mass Spectrometry 2004, 15:1572-1580.
47. Senyo S.E., Steinhauser M.L., Pizzimenti C.L., Yang V.K., Cai L., Wang M., et al. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013, 493:433-436.
48. Cabin-Flaman A., Monnier A.F., Coffinier Y., Audinot J.N., Gibouin D., Wirtz T., et al. Combed single DNA molecules imaged by secondary ion mass spectrometry. Analytical Chemistry 2011, 83:6940-6947.
49. Potten C.S., Hume W.J., Reid P., Cairns J. The segregation of DNA in epithelial stem cells. Cell 1978, 15:899-906.
50. Quyn A.J., Appleton P.L., Carey F.A., Steele R.J., Barker N., Clevers H., et al. Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 2010, 6:175-181.
51. Shinin V., Gayraud-Morel B., Gomes D., Tajbakhsh S. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nature Cell Biology 2006, 8:677-687.
52. Conboy M.J., Karasov A.O., Rando T.A. High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biology 2007, 5:e102.
53. Falconer E., Chavez E.A., Henderson A., Poon S.S., McKinney S., Brown L., et al. Identification of sister chromatids by DNA template strand sequences. Nature 2010, 463:93-97.
54. Neese R.A., Misell L.M., Turner S., Chu A., Kim J., Cesar D., et al. Measurement in vivo of proliferation rates of slow turnover cells by 2H2O labeling of the deoxyribose moiety of DNA. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:15345-15350.
55. Pittet M.J., Weissleder R. Intravital imaging. Cell 2011, 147:983-991.
56. Kuypers M.M. Microbiology. Sizing up the uncultivated majority. Science 2007, 317:1510-1511.
57. Musat N., Foster R., Vagner T., Adam B., Kuypers M.M. Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiology Review 2012, 36:486-511.