Quantitative in vivo characterization of intracellular and extracellular pH profiles in heterogeneous tumors: A novel method enabling multiparametric pH analysis

Cancer Research

Volumn 73, Issue 15, 2013, Pages 4616-4628

  Lutz, Norbert W ^a   Fur, Yann Le ^a   Chiche, Johanna ^b,d   Pouysse, Jacqueśgur ^b,c   Cozzone, Patrick J ^a  

^a University of Aix Marseille   (France)

^b UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^c CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOPROPANEPHOSPHONIC ACID; PHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PH; COMPUTER SIMULATION; MOUSE; NONHUMAN; PHANTOM; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT;

ANIMALS; CRICETINAE; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MICE; NEOPLASMS, EXPERIMENTAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84881473550     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-0767     Document Type: Article

References (42)

1. Helmlinger G, Yuan F, Dellian M, Jain RK. Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 1997;3:177-82.
2. Kobus T, Bitz AK, van Uden MJ, LagemaatMW,Rothgang E, Orzada S, et al. In vivo 31P MR spectroscopic imaging of the human prostate at 7 T: safety and feasibility. Magn Reson Med 2012;68:1683-95.
3. Vandenborne K, McCully K, Kakihira H, Prammer M, Bolinger L, Detre JA, et al. Metabolic heterogeneity in human calf muscle during maximal exercise. Proc Natl Acad Sci U S A 1991;88:5714-8.
4. Rossiter HB, Ward SA, Howe FA, Kowalchuk JM, Griffiths JR, Whipp BJ. Dynamics of intramuscular 31P-MRS P(i) peak splitting and the slowcomponents of PCr andO2 uptake during exercise. J Appl Physiol 2002;93:2059-69.
5. Ackerman JJ, Soto GE, Spees WM, Zhu Z, Evelhoch JL. The NMR chemical shift pH measurement revisited: analysis of error and modeling of a pH dependent reference. Magn Reson Med 1996;36:674-83.
6. Moon RB, Richards JH. Determination of intracellular pH by 31P magnetic resonance. J Biol Chem 1973;248:7276-8.
7. Griffiths JR, Stevens AN, Iles RA, Gordon RE, Shaw D. 31P-NMR investigation of solid tumours in the living rat. Biosci Rep 1981;1: 319-25.
8. Gillies RJ, Liu Z, Bhujwalla ZM. 31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate. Am J Physiol 1994;36:C195-203.
9. Raghunand N. Tissue pH measurement by magnetic resonance spectroscopy and imaging. Methods Mol Med 2006;124:347-64.
10. Madden A, Glaholm J, Leach MO. An assessment of the sensitivity of in vivo 31P nuclear magnetic resonance spectroscopy as a means of detecting pH heterogeneity in tumours: a simulation study. Br J Radiol 1990;63:120-4.
11. Viola A, Lutz NW, Maroc C, Chabannon C, Julliard M, Cozzone PJ. Metabolic effects of photodynamically induced apoptosis in an erythroleukemic cell line. A (31)P NMR spectroscopic study of Victoria- Blue-BO-sensitized TF-1 cells. Int J Cancer 2000;85:733-9.
12. Sokal RR, Rohlf FJ. Biometry, 3rd ed. New York: Freeman; 1995.
13. Doane DP, Seward LE. Measuring skewness: a forgotten statistic? J Stat Educ 2011;19:1-18.
14. Cover TM, Thomas JA. Elements of information theory. New York: Wiley; 1991.
15. Lesne A. Statistical entropy: at the crossroads between probability, information theory, dynamical systems and statistical physics. Math Struct Comp Sci. In press.
16. Chiche J, Fur YL, Vilmen C, Frassineti F, Daniel L, Halestrap AP, et al. In vivo pH in metabolic-defective Ras-transformed fibroblast tumors: key role of the monocarboxylate transporter, MCT4, for inducing an alkaline intracellular pH. Int J Cancer 2012;130:1511-20.
17. Sauter R, Mueller S, Weber H. Localization in in vivo 31P NMR spectroscopy by combining surface coils and slice-selective saturation. J Magn Reson 1987;75:167-73.
18. Lutz NW, Cozzone PJ. Multiparametric optimization of (31)P NMR spectroscopic analysis of phospholipids in crude tissue extracts. 1. Chemical shift and signal separation. Anal Chem 2010;82:5433-40.
19. Lutz NW, Cozzone PJ. Multiparametric optimization of (31)P NMR spectroscopic analysis of phospholipids in crude tissue extracts. 2. Line width and spectral resolution. Anal Chem 2010;82:5441-6.
20. Lutz NW, Cozzone PJ. Phospholipidomics by phosphorus nuclear magnetic resonance spectroscopy of tissue extracts. In:Lutz NW, Sweedler JV, Wevers RA, editors. Methodologies for metabolomics. New York: Cambridge University Press; 2013. p. 377-414.
21. Le Fur Y, Nicoli F, Guye M, Confort-Gouny S, Cozzone PJ, Kober F. Grid-free interactive and automated data processing for MR chemical shift imaging data. Magma 2010;23:23-30.
22. He K, Meeden G. Selecting the number of bins in a histogram: a decision theoretic approach. J Stat Plan Inference 1997;61:49-59.
23. Hargas L, Koniar D, Stofan S. Sophisticated biomedical tissue measurement using image analysis and virtual instrumentation. In:Folea S, editor. Practical applications and solutions using Labview software. Rijeka, Croatia: InTech; 2011.
24. Kohler U, Kreuter F. Data analysis using stata. College Station, TX: Stata Press; 2005.
25. Frigg R, Werndl C. Entropy: a guide for the perplexed. In:Beisbart C, Hartmann S, editors. Probabilities in physics. Oxford, UK: Oxford University Press; 2011.
26. Güçlü B. Maximizing the entropy of histogram bar heights to explore neural activity: a simulation study on auditory and tactile fibers. Acta Neurobiol Exp 2005;65:399-407.
27. Park HM. Univariate analysis and normality test using SAS, Stata, and SPSS. Bloomington: the University Information Technology Services (UITS) Center for Statistical and Mathematical Computing, Indiana University, 2008.
28. Graham RA, Taylor AH, Brown TR. A method for calculating the distribution of pH in tissues and a new source of pH error from the 31P-NMR spectrum. Am J Physiol 1994;266:R638-45.
29. Marshall I, Higinbotham J, Bruce S, Freise A. Use of Voigt lineshape for quantification of in vivo 1H spectra. Magn Reson Med 1997;37:651-7.
30. Jensen PA, Bard JF. Operations research models and methods. Vol. Supplementary material. Hoboken, NJ: Wiley; 2003. Available from: http://www.me.utexas.edu/-jensen/ORMM.
31. DeCarlo LT. On the meaning and use of kurtosis. Psychol Methods 1997;2:292-307.
32. Lin Y, Wu TY, Gmitro AF. Error analysis of ratiometric imaging of extracellular pH in a window chamber model. J Biomed Opt 2012; 17:046004.
33. Hak S, Reitan NK, Haraldseth O, de Lange Davies C. Intravital microscopy in window chambers: a unique tool to study tumor angiogenesis and delivery of nanoparticles. Angiogenesis 2010;13:113-30.
34. Garcia-Martin ML, Herigault G, Remy C, Farion R, Ballesteros P, Coles JA, et al. Mapping extracellular pH in rat brain gliomas in vivo by 1H magnetic resonance spectroscopic imaging: comparison withmaps of metabolites. Cancer Res 2001;61:6524-31.
35. Provent P, Benito M, Hiba B, Farion R, Lopez-Larrubia P, Ballesteros P, et al. Serial in vivo spectroscopic nuclear magnetic resonance imaging of lactate and extracellular pH in rat gliomas shows redistribution of protons away from sites of glycolysis. Cancer Res 2007;67:7638-45.
36. Garcia-Martin ML, Martinez GV, Raghunand N, Sherry AD, Zhang S, Gillies RJ. High resolution pH(e) imaging of rat glioma using pH-dependent relaxivity. Magn Reson Med 2006;55: 309-15.
37. Liu G, Li Y, Sheth VR, Pagel MD. Imaging in vivo extracellular pH with a single paramagnetic chemical exchange saturation transfer magnetic resonance imaging contrast agent. Mol Imaging 2012;11:47-57.
38. Gallagher FA, Kettunen MI, Brindle KM. Imaging pH with hyperpolarized 13C. NMR Biomed 2011;24:1006-15.
39. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989;49:6449-65.
40. Glunde K, Shah T, Winnard PT Jr, Raman V, Takagi T, Vesuna F, et al. Hypoxia regulates choline kinase expression through hypoxia-inducible factor-1 alpha signaling in a human prostate cancer model. Cancer Res 2008;68:172-80.
41. Lutz NW, Sweedler JV, Wevers RA, editors. Methodologies for metabolomics. New York: Cambridge University Press; 2013.
42. Lope-Piedrafita S, Garcia-Martin ML, Galons JP, Gillies RJ, Trouard TP. Longitudinal diffusion tensor imaging in a rat brain glioma model. NMR Biomed 2008;21:799-808.