Imaging pH and metastasis

NMR in Biomedicine

Volumn 24, Issue 6, 2011, Pages 582-591

  Hashim, Arig Ibrahim ^a   Zhang, Xiaomeng ^a   Wojtkowiak, Jonathan W ^a   Martinez, Gary V ^a   Gillies, Robert J ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Metastasis; Tumor microenvironment; Tumor pH

Indexed keywords

ACIDIC PH; BASEMENT MEMBRANE; CANCER PROGRESSION; EXTRACELLULAR PH; KEY FACTORS; METASTASIS; MICROENVIRONMENTS; MULTIPLE INTERACTIONS; MULTISTEP PROCESS; NORMAL TISSUE; POOR PERFUSION; SIGNIFICANT IMPACTS; SOLID TUMORS; TUMOR CELLS; TUMOR DEVELOPMENT; TUMOR MICROENVIRONMENT;

BLOOD; DISEASES; ENZYME ACTIVITY; TUMORS;

PATHOLOGY;

2 IMIDAZOLE 1 YL 3 ETHOXYCARBONYLPROPIONIC ACID; 3 [N (4 FLUOR 2 TRIFLUOROMETHYL PHENYL) SULPHAMOYL] PROPIONIC ACID; 3 AMINOPROPYLPHOSPHONATE; BICARBONATE; BICARBONATE C 13; CATHEPSIN B; CATHEPSIN L; GADOTERIC ACID; GELATINASE A; GELATINASE B; NUCLEAR MAGNETIC RESONANCE IMAGING AGENT; PHOSPHATE; PROTON PUMP INHIBITOR; PYRIDOXINE DERIVATIVE; UNCLASSIFIED DRUG; ZK 150471;

ACIDIFICATION; BIOLUMINESCENCE; BREAST CANCER; CARBON NUCLEAR MAGNETIC RESONANCE; CELL PROLIFERATION; CHEMICAL ANALYSIS; CHEMICAL EXCHANGE SATURATION TRANSFER; CIRCULATING TUMOR CELL; COMPETITIVE INHIBITION; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DRUG DISTRIBUTION; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FLUORINE NUCLEAR MAGNETIC RESONANCE; HUMAN; HYDROGEN BOND; ISOTOPE LABELING; LACTIC ACIDOSIS; LUNG METASTASIS; MAJOR HISTOCOMPATIBILITY COMPLEX; METASTASIS; MICROMETASTASIS; MOLECULAR IMAGING; MOLECULAR PROBE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROSTATE CANCER; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SIGNAL NOISE RATIO; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SOLID TUMOR; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

ANIMALS; HUMANS; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE IMAGING; MODELS, BIOLOGICAL; NEOPLASM METASTASIS;

EID: 79960825218     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.1644     Document Type: Review

References (77)

1. Ruoslahti E.How cancer spreads.Sci. Am. 1996;275:72-77.
2. Allard WJ, Matera J, Miller MC, Repollet M, Connelly MC, Rao C, Tibbe AG, Uhr JW, Terstappen LW.Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases.Clin. Cancer Res. 2004;10:6897-6904.
3. Tannock IF, Rotin D.Acid pH in tumors and its potential for therapeutic exploitation.Cancer research 1989;49(16):4373-4384.
4. Gatenby RA, Gawlinski ET.A reaction-diffusion model of cancer invasion.Cancer Res. 1996;56:5745-5753.
5. Stubbs M, McSheehy PM, Griffiths JR, Bashford CL.Causes and consequences of tumour acidity and implications for treatment.Mol. Med. Today 2000;6:15-19.
6. Dellian M, Helmlinger G, Yuan F, Jain RK.Fluorescence ratio imaging of interstitial pH in solid tumours: effect of glucose on spatial and temporal gradients.Br. J. Cancer 1996;74:1206-1215.
7. Jahde E, Rajewsky MF.Tumor-selective modification of cellular microenvironment in vivo: effect of glucose infusion on the pH in normal and malignant rat tissues.Cancer Res. 1982;42:1505-1512.
8. Volk T, Jahde E, Fortmeyer HP, Glusenkamp KH, Rajewsky MF.pH in human tumour xenografts: effect of intravenous administration of glucose.Br. J. Cancer 1993;68:492-500.
9. Jain RK, Shah SA, Finney PL.Continuous noninvasive monitoring of pH and temperature in rat Walker 256 carcinoma during normoglycemia and hyperglycemia.J. Natl. Cancer Inst. 1984;73:429-436.
10. Mazzio EA, Smith B, Soliman KF.Evaluation of endogenous acidic metabolic products associated with carbohydrate metabolism in tumor cells.Cell. Biol. Toxicol. 2010;26:177-188.
11. Walenta S, Wetterling M, Lehrke M, Schwickert G, Sundfor K, Rofstad EK, Mueller-Klieser W.High lactate levels predict likelihood of metastases, tumor recurrence, and restricted patient survival in human cervical cancers.Cancer Res. 2000;60:916-921.
12. Schwickert G, Walenta S, Sundfor K, Rofstad EK, Mueller-Klieser W.Correlation of high lactate levels in human cervical cancer with incidence of metastasis.Cancer Res. 1995;55:4757-4759.
13. Newell K, Franchi A, Pouyssegur J, Tannock I.Studies with glycolysis-deficient cells suggest that production of lactic acid is not the only cause of tumor acidity.Proc. Natl. Acad. Sci. U.S.A. 1993;90:1127-1131.
14. Helmlinger G, Sckell A, Dellian M, Forbes NS, Jain RK.Acid production in glycolysis-impaired tumors provides new insights into tumor metabolism.Clin. Cancer Res. 2002;8:1284-1291.
15. Robergs RA, Ghiasvand F, Parker D.Biochemistry of exercise-induced metabolic acidosis.Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004;287:R502-516.
16. Gatenby RA, Gillies RJ.Why do cancers have high aerobic glycolysis?Nat. Rev. Cancer 2004;4:891-899.
17. Svastova E, Hulikova A, Rafajova M, Zat'ovicova M, Gibadulinova A, Casini A, Cecchi A, Scozzafava A, Supuran CT, Pastorek J, Pastorekova S.Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH.FEBS Lett. 2004;577:439-445.
18. Chen JL, Lucas JE, Schroeder T, Mori S, Wu J, Nevins J, Dewhirst M, West M, Chi JT.The genomic analysis of lactic acidosis and acidosis response in human cancers.PLoS Genet. 2008;4:e1000293.
19. Walenta S, Schroeder T, Mueller-Klieser W.Lactate in solid malignant tumors: potential basis of a metabolic classification in clinical oncology.Curr. Med. Chem. 2004;11:2195-2204.
20. Gillies RJ, Raghunand N, Garcia-Martin ML, Gatenby RA.pH imaging. A review of pH measurement methods and applications in cancers.IEEE Eng. Med. Biol. Mag. 2004;23:57-64.
21. Zhang X, Lin Y, Gillies RJ.Tumor pH and its measurement.J. Nucl. Med. 2010;51:1167-1170.
22. Gillies RJ, Liu Z, Bhujwalla Z.31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate.Am. J. Physiol. 1994;267:C195-203.
23. Soto GE, Zhu Z, Evelhoch JL, Ackerman JJ.Tumor 31P NMR pH measurements in vivo: a comparison of inorganic phosphate and intracellular 2-deoxyglucose-6-phosphate as pHnmr indicators in murine radiation-induced fibrosarcoma-1.Magn. Reson. Med. 1996;36:698-704.
24. Gillies RJ, Ogino T, Shulman RG, Ward DC.31P nuclear magnetic resonance evidence for the regulation of intracellular pH by Ehrlich ascites tumor cells.J. Cell Biol. 1982;95:24-28.
25. 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;63:120-124.
26. Szwergold BS.NMR spectroscopy of cells.Annu. Rev. Physiol. 1992;54:775-798.
27. Bhujwalla ZM, McCoy CL, Glickson JD, Gillies RJ, Stubbs M.Estimations of intra- and extracellular volume and pH by 31P magnetic resonance spectroscopy: effect of therapy on RIF-1 tumours.Br. J. Cancer 1998;78:606-611.
28. Raghunand N, Altbach MI, van Sluis R, Baggett B, Taylor CW, Bhujwalla ZM, Gillies RJ.Plasmalemmal pH-gradients in drug-sensitive and drug-resistant MCF-7 human breast carcinoma xenografts measured by 31P magnetic resonance spectroscopy.Biochem. Pharmacol. 1999;57:309-312.
29. Hunjan S, Mason RP, Mehta VD, Kulkarni PV, Aravind S, Arora V, Antich PP.Simultaneous intracellular and extracellular pH measurement in the heart by 19F NMR of 6-fluoropyridoxol.Magn. Reson. Med. 1998;39:551-556.
30. Ojugo AS, McSheehy PM, McIntyre DJ, McCoy C, Stubbs M, Leach MO, Judson IR, Griffiths JR.Measurement of the extracellular pH of solid tumours in mice by magnetic resonance spectroscopy: a comparison of exogenous (19)F and (31)P probes.NMR Biomed. 1999;12:495-504.
31. Rabenstein DL, Isab AA.Determination of the intracellular pH of intact erythrocytes by 1H NMR spectroscopy.Anal. Biochem. 1982;121:423-432.
32. Gil S, Zaderenzo P, Cruz F, Cerdán S, Ballesteros P.Imidazol-1-ylalkanoic acids as extrinsic 1H NMR probes for the determination of intracellular pH, extracellular pH and cell volume.Bioorg. Med. Chem. 1994;2:305-314.
33. van Sluis R, Bhujwalla ZM, Raghunand N, Ballesteros P, Alvarez J, Cerdan S, Galons JP, Gillies RJ.In vivo imaging of extracellular pH using 1H MRSI.Magn. Reson. Med. 1999;41:743-750.
34. Garcia-Martin ML, Herigault G, Remy C, Farion R, Ballesteros P, Coles JA, Cerdan S, Ziegler A.Mapping extracellular pH in rat brain gliomas in vivo by 1H magnetic resonance spectroscopic imaging: comparison with maps of metabolites.Cancer Res. 2001;61:6524-6531.
35. Provent P, Benito M, Hiba B, Farion R, Lopez-Larrubia P, Ballesteros P, Remy C, Segebarth C, Cerdan S, Coles JA, Garcia-Martin ML.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;67:7638-7645.
36. Hoffman DW, Henkens RW.The rates of fast reactions of carbon dioxide and bicarbonate in human erythrocytes measured by carbon-13 NMR.Biochem. Biophys. Res. Commun. 1987;143:67-73.
37. Arús C, Chang YC, Bárány M.The separation of phosphocreatine from creatine, and pH determination in frog muscle by natural abundance 13C-NMR.Biochim. Biophys. Acta 1985;844:91-93.
38. Gallagher FA, Kettunen MI, Day SE, Hu DE, Ardenkjaer-Larsen JH, Zandt R, Jensen PR, Karlsson M, Golman K, Lerche MH, Brindle KM.Magnetic resonance imaging of pH in vivo using hyperpolarized 13C-labelled bicarbonate.Nature 2008;453:940-943.
39. Schroeder MA, Swietach P, Atherton HJ, Gallagher FA, Lee P, Radda GK, Clarke K, Tyler DJ.Measuring intracellular pH in the heart using hyperpolarized carbon dioxide and bicarbonate: a 13C and 31P magnetic resonance spectroscopy study.Cardiovasc. Res. 2010;86:82-91.
40. Mikawa M, Miwa N, Bräutigam M, Akaike T, Maruyama A.Gd(3+)-loaded polyion complex for pH depiction with magnetic resonance imaging.J. Biomed. Mater. Res. 2000;49:390-395.
41. Lowe MP, Parker D, Reany O, Aime S, Botta M, Castellano G, Gianolio E, Pagliarin R.pH-dependent modulation of relaxivity and luminescence in macrocyclic gadolinium and europium complexes based on reversible intramolecular sulfonamide ligation.J. Am. Chem. Soc. 2001;123:7601-7609.
42. Zhang S, Wu K, Sherry A.A novel ph-sensitive MRI contrast agent.Angew. Chem. Int. Ed. Engl. 1999;38:3192-3194.
43. Beauregard DA, Parker D, Brindle KM.Relaxation-based mapping of tumour pH.Proceedings of the 6th Annual Meeting of ISMRM, Sydney, Australia, 1998;53.
44. Raghunand N, Howison C, Sherry AD, Zhang S, Gillies RJ.Renal and systemic pH imaging by contrast-enhanced MRI.Magn. Reson. Med. 2003;49:249-257.
45. 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;55:309-315.
46. Zhang X, Martinez GV, Garcia-Martin ML, Woods M, Sherry D, Gillies RJ.High spatio-temporal resolution pHe mapping of a rat glioma derived from pH-dependent spin-lattice relaxivity.Proceedings of the 16th Annual Meeting of ISMRM, Toronto, Ontario, Canada, 2008;370.
47. Sherry AD, Woods M.Chemical exchange saturation transfer contrast agents for magnetic resonance imaging.Annu. Rev. Biomed. Eng. 2008;10:391-411.
48. Hwang TL, van Zijl PC, Mori S.Accurate quantitation of water-amide proton exchange rates using the phase-modulated CLEAN chemical EXchange (CLEANEX-PM) approach with a Fast-HSQC (FHSQC) detection scheme.J. Biomol. NMR 1998;11:221-226.
49. Snoussi K, Bulte JWM, Guéron M, van Zijl PCM.Sensitive CEST agents based on nucleic acid imino proton exchange: detection of poly(rU) and of a dendrimer-poly(rU) model for nucleic acid delivery and pharmacology.Magn. Reson. Med. 2003;49:998-1005.
50. Zhang S, Merritt M, Woessner DE, Lenkinski RE, Sherry AD.PARACEST agents: modulating MRI contrast via water proton exchange.Acc. Chem. Res. 2003;36:783-790.
51. Aime S, Barge A, Delli Castelli D, Fedeli F, Mortillaro A, Nielsen FU, Terreno E.Paramagnetic lanthanide(III) complexes as pH-sensitive chemical exchange saturation transfer (CEST) contrast agents for MRI applications.Magn. Reson. Med. 2002;47:639-648.
52. Zhou J, Lal B, Wilson DA, Laterra J, van Zijl PCM.Amide proton transfer (APT) contrast for imaging of brain tumors.Magn. Reson. Med. 2003;50:1120-1126.
53. Liu G, Li Y, Pagel M.A Single PARACEST MRI Contrast Agent for Accurate In Vivo pH Measurements.Proceedings of the 15th Annual Meeting of ISMRM, Berlin, Germany, 2007;3406.
54. Resel Folkersma L, Olivier Gomez C, San Jose Manso L, Veganzones de Castro S, Galante Romo I, Vidaurreta Lazaro M, de la Orden GV, Arroyo Fernandez M, Diaz Rubio E, Silmi Moyano A, Maestro de Las Casas MA.Immunomagnetic quantification of circulating tumoral cells in patients with prostate cancer: clinical and pathological correlation.Arch. Esp. Urol. 2010;63:23-31.
55. Xu L, Fidler IJ.Acidic pH-induced elevation in interleukin 8 expression by human ovarian carcinoma cells.Cancer Res. 2000;60:4610-4616.
56. Fukumura D, Xu L, Chen Y, Gohongi T, Seed B, Jain RK.Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo.Cancer Res. 2001;61:6020-6024.
57. Scott PA, Gleadle JM, Bicknell R, Harris AL.Role of the hypoxia sensing system, acidity and reproductive hormones in the variability of vascular endothelial growth factor induction in human breast carcinoma cell lines.Int. J. Cancer 1998;75:706-712.
58. Xu L, Fukumura D, Jain RK.Acidic extracellular pH induces vascular endothelial growth factor (VEGF) in human glioblastoma cells via ERK1/2 MAPK signaling pathway: mechanism of low pH-induced VEGF.J. Biol. Chem. 2002;277:11368-11374.
59. Rofstad EK, Mathiesen B, Kindem K, Galappathi K.Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice.Cancer Res. 2006;66:6699-6707.
60. Moellering RE, Black KC, Krishnamurty C, Baggett BK, Stafford P, Rain M, Gatenby RA, Gillies RJ.Acid treatment of melanoma cells selects for invasive phenotypes.Clin. Exp. Metastasis 2008;25:411-425.
61. Blum G, von Degenfeld G, Merchant MJ, Blau HM, Bogyo M.Noninvasive optical imaging of cysteine protease activity using fluorescently quenched activity-based probes.Nat. Chem. Biol. 2007;3:668-677.
62. Yang Y, Hong H, Zhang Y, Cai W.Molecular imaging of proteases in cancer.Cancer Growth Metastasis 2009;2:13-27.
63. Fidler IJ.Cancer metastasis.Br. Med. Bull. 1991;47:157-177.
64. Kienast Y, von Baumgarten L, Fuhrmann M, Klinkert WE, Goldbrunner R, Herms J, Winkler F.Real-time imaging reveals the single steps of brain metastasis formation.Nature Medicine 2010;16:116-122.
65. Robey IF, Baggett BK, Kirkpatrick ND, Roe DJ, Dosescu J, Sloane BF, Hashim AI, Morse DL, Raghunand N, Gatenby RA, Gillies RJ.Bicarbonate increases tumor pH and inhibits spontaneous metastases.Cancer Res. 2009;69:2260-2268.
66. Blick T, Widodo E, Hugo H, Waltham M, Lenburg ME, Neve RM, Thompson EW.Epithelial mesenchymal transition traits in human breast cancer cell lines.Clin. Exp. Metastasis 2008;25:629-642.
67. Trimboli AJ, Fukino K, de Bruin A, Wei G, Shen L, Tanner SM, Creasap N, Rosol TJ, Robinson ML, Eng C, Ostrowski MC, Leone G.Direct evidence for epithelial-mesenchymal transitions in breast cancer.Cancer Res. 2008;68:937-945.
68. Agiostratidou G, Hulit J, Phillips GR, Hazan RB.Differential cadherin expression: potential markers for epithelial to mesenchymal transformation during tumor progression.J. Mammary Gland Biol. Neoplasia 2007;12:127-133.
69. Guarino M, Rubino B, Ballabio G.The role of epithelial-mesenchymal transition in cancer pathology.Pathology 2007;39:305-318.
70. Chen KH, Tung PY, Wu JC, Chen Y, Chen PC, Huang SH, Wang SM.An acidic extracellular pH induces Src kinase-dependent loss of beta-catenin from the adherens junction.Cancer Lett. 2008;267:37-48.
71. Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, Edinger M, Gottfried E, Schwarz S, Rothe G, Hoves S, Renner K, Timischl B, Mackensen A, Kunz-Schughart L, Andreesen R, Krause SW, Kreutz M.Inhibitory effect of tumor cell-derived lactic acid on human T cells.Blood 2007;109:3812-3819.
72. Fischer B, Muller B, Fisch P, Kreutz W.An acidic microenvironment inhibits antitumoral non-major histocompatibility complex-restricted cytotoxicity: implications for cancer immunotherapy.J. Immunother. 2000;23:196-207.
73. Bosticardo M, Ariotti S, Losana G, Bernabei P, Forni G, Novelli F.Biased activation of human T lymphocytes due to low extracellular pH is antagonized by B7/CD28 costimulation.Eur. J. Immunol. 2001;31:2829-2838.
74. Dietl K, Renner K, Dettmer K, Timischl B, Eberhart K, Dorn C, Hellerbrand C, Kastenberger M, Kunz-Schughart LA, Oefner PJ, Andreesen R, Gottfried E, Kreutz MP.Lactic acid and acidification inhibit TNF secretion and glycolysis of human monocytes.J Immunol 2010;184(3):1200-1209.
75. De Milito A, Canese R, Marino ML, Borghi M, Iero M, Villa A, Venturi G, Lozupone F, Iessi E, Logozzi M, Della Mina, P, Santinami M, Rodolfo M, Podo F, Rivoltini L, Fais S.pH-dependent antitumor activity of proton pump inhibitors against human melanoma is mediated by inhibition of tumor acidity.Int. J. Cancer 2010;127(1):207-219.
76. Raghunand N, He X, van Sluis R, Mahoney B, Baggett B, Taylor CW, Paine-Murrieta G, Roe D, Bhujwalla ZM, Gillies RJ.Enhancement of chemotherapy by manipulation of tumour pH.Br. J. Cancer 1999;80:1005-1011.
77. Silva AS, Yunes JA, Gillies RJ, Gatenby RA.The potential role of systemic buffers in reducing intratumoral extracellular pH and acid-mediated invasion.Cancer Res. 2009;69:2677-2684.