Oncogene pathway activation in mammary tumors dictates FDG-PET uptake

Cancer Research

Volumn 74, Issue 24, 2014, Pages 7583-7598

  Alvarez, James V ^a,b   Belka, George K ^a,b   Pan, Tien Chi ^a,b   Chen, Chien Chung ^a,b   Blankemeyer, Eric ^b   Alavi, Abass ^b   Karp, Joel S ^b   Chodosh, Lewis A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORODEOXYGLUCOSE F 18; GLUCOSE TRANSPORTER 1; HEXOKINASE 1; HK2 PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; TUMOR PROTEIN; UNCLASSIFIED DRUG; GLUCOSE; HEXOKINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST TUMOR; CONTROLLED STUDY; DOWN REGULATION; DRUG UPTAKE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GLUT1 GENE; GLYCOLYSIS; HK1 GENE; HK2 GENE; MOUSE; NONHUMAN; ONCOGENE; POSITRON EMISSION TOMOGRAPHY; SIGNAL TRANSDUCTION; TUMOR GENE; TUMOR GROWTH; ANIMAL; BIOSYNTHESIS; CELL PROLIFERATION; FEMALE; GENETICS; HUMAN; MAMMARY NEOPLASMS, ANIMAL; METABOLISM; PATHOLOGY;

ANIMALS; CELL PROLIFERATION; FEMALE; FLUORODEOXYGLUCOSE F18; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; HEXOKINASE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MAMMARY NEOPLASMS, ANIMAL; MICE; NEOPLASM PROTEINS; POSITRON-EMISSION TOMOGRAPHY;

EID: 84917708633     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1235     Document Type: Article

References (54)

1. Kim JW, Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res 2006;66:8927-30.
2. Mankoff DA, Eubank WB. Current and future use of positron emission tomography (PET) in breast cancer. J Mammary Gland Biol Neoplasia 2006;11:125-36.
3. Oshida M, Uno K, Suzuki M, Nagashima T, Hashimoto H, Yagata H, et al. Predicting the prognoses of breast carcinoma patients with positron emission tomography using 2-deoxy-2-fluoro[18F]-D-glucose. Cancer 1998;82:2227-34.
4. Mankoff DA, Dunnwald LK, Gralow JR, Ellis GK, Charlop A, Lawton TJ, et al. Blood flow and metabolism in locally advanced breast cancer: relationship to response to therapy. J Nucl Med 2002;43:500-9.
5. Inoue T, Yutani K, Taguchi T, Tamaki Y, Shiba E, Noguchi S. Preoperative evaluation of prognosis in breast cancer patients by [(18)F]2-Deoxy-2-fluoro-D-glucose-positron emission tomography. J Cancer Res Clin Oncol 2004;130:273-8.
6. Wahl RL, Zasadny K, Helvie M, Hutchins GD, Weber B, Cody R. Metabolic monitoring of breast cancer chemohormonotherapy using positron emission tomography: initial evaluation. J Clin Oncol 1993;11:2101-11.
7. Mankoff DA, Dunnwald LK. Changes in glucose metabolism and blood flow following chemotherapy for breast cancer. PET Clinics 2006;1:71-81.
8. Schelling M, Avril N, Nahrig J, Kuhn W, Romer W, Sattler D, et al. Positron emission tomography using [(18)F]Fluorodeoxyglucose for monitoring primary chemotherapy in breast cancer. J Clin Oncol 2000;18:1689-95.
9. Smith IC, Welch AE, Hutcheon AW, Miller ID, Payne S, Chilcott F, et al. Positron emission tomography using [(18)F]-fluorodeoxy-D-glucose to predict the pathologic response of breast cancer to primary chemotherapy. J Clin Oncol 2000;18:1676-88.
10. Avril N, Menzel M, Dose J, Schelling M, Weber W, Janicke F, et al. Glucose metabolism of breast cancer assessed by 18F-FDG PET: histologic and immunohistochemical tissue analysis. J Nucl Med 2001;42:9-16.
11. Adler LP, Crowe JP, al-Kaisi NK, Sunshine JL. Evaluation of breast masses and axillary lymph nodes with [F-18] 2-deoxy-2-fluoro-Dglucose PET. Radiology 1993;187:743-50.
12. Crippa F, Seregni E, Agresti R, Chiesa C, Pascali C, Bogni A, et al. Association between [18F]fluorodeoxyglucose uptake and postoperative histopathology, hormone receptor status, thymidine labelling index and p53 in primary breast cancer: a preliminary observation. Eur J Nucl Med 1998;25:1429-34.
13. Bos R, van Der Hoeven JJ, van Der Wall E, van Der Groep P, van Diest PJ, Comans EF, et al. Biologic correlates of (18) fluorodeoxyglucose uptake in human breast cancer measured by positron emission tomography. J Clin Oncol 2002;20:379-87.
14. Scheepers A, Joost HG, Schurmann A. The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function. JPEN J Parenter Enteral Nutr 2004;28:364-71.
15. Bormans GM, Van Oosterwyck G, De Groot TJ, Veyhl M, Mortelmans L, Verbruggen AM, et al. Synthesis and biologic evaluation of (11)c-methyl-D-glucoside, a tracer of the sodium-dependent glucose transporters. J Nucl Med 2003;44:1075-81.
16. Brown RS, Goodman TM, Zasadny KR, Greenson JK, Wahl RL. Expression of hexokinase II and Glut-1 in untreated human breast cancer. Nucl Med Biol 2002;29:443-53.
17. de Geus-Oei LF, van Krieken JH, Aliredjo RP, Krabbe PF, Frielink C, Verhagen AF, et al. Biological correlates of FDG uptake in non-small cell lung cancer. Lung Cancer 2007;55:79-87.
18. Mamede M, Higashi T, Kitaichi M, Ishizu K, Ishimori T, Nakamoto Y, et al. [18F]FDG uptake and PCNA, Glut-1, and hexokinase-II expressions in cancers and inflammatory lesions of the lung. Neoplasia 2005;7:369-79.
19. Chung JK, Lee YJ, Kim SK, Jeong JM, Lee DS, Lee MC. Comparison of [18F]fluorodeoxyglucose uptake with glucose transporter-1 expression and proliferation rate in human glioma and non-small-cell lung cancer. Nucl Med Commun 2004;25:11-7.
20. Marom EM, Aloia TA, Moore MB, Hara M, Herndon JE II, Harpole DH Jr, et al. Correlation of FDG-PET imaging with Glut-1 and Glut-3 expression in early-stage non-small cell lung cancer. Lung Cancer 2001;33:99-107.
21. Kurokawa T, Yoshida Y, Kawahara K, Tsuchida T, Okazawa H, Fujibayashi Y, et al. Expression of GLUT-1 glucose transfer, cellular proliferation activity and grade of tumor correlate with [F-18]-fluorodeoxyglucose uptake by positron emission tomography in epithelial tumors of the ovary. Int J Cancer 2004;109:926-32.
22. Higashi T, Saga T, Nakamoto Y, Ishimori T, Mamede MH, Wada M, et al. Relationship between retention index in dual-phase (18)F-FDG PET, and hexokinase-II and glucose transporter-1 expression in pancreatic cancer. J Nucl Med 2002;43:173-80.
23. Riedl CC, Akhurst T, Larson S, Stanziale SF, Tuorto S, Bhargava A, et al. 18F-FDG PET scanning correlates with tissue markers of poor prognosis and predicts mortality for patients after liver resection for colorectal metastases. J Nucl Med 2007;48:771-5.
24. Paudyal B, Oriuchi N, Paudyal P, Higuchi T, Nakajima T, Endo K. Expression of glucose transporters and hexokinase II in cholangiocellular carcinoma compared using [18F]-2-fluro-2-deoxy-D-glucose positron emission tomography. Cancer Sci 2008;99:260-6.
25. Tohma T, Okazumi S, Makino H, Cho A, Mochiduki R, Shuto K, et al. Relationship between glucose transporter, hexokinase and FDG-PET in esophageal cancer. Hepatogastroenterology 2005;52:486-90.
26. Tian M, Zhang H, Higuchi T, Oriuchi N, Nakasone Y, Takata K, et al. Hexokinase-II expression in untreated oral squamous cell carcinoma: comparison with FDG PET imaging. Ann Nucl Med 2005;19:335-8.
27. Dang CV, Semenza GL. Oncogenic alterations of metabolism. Trends Biochem Sci 1999;24:68-72.
28. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008;7:11-20.
29. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009;324:1029-33.
30. Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell 2008;134:703-7.
31. Rathmell JC, Fox CJ, Plas DR, Hammerman PS, Cinalli RM, Thompson CB. Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival. Mol Cell Biol 2003;23:7315-28.
32. Gordan JD, Thompson CB, Simon MC. HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer cell 2007;12:108-13.
33. Biaglow JE, Cerniglia G, Tuttle S, Bakanauskas V, Stevens C, McKenna G. Effect of oncogene transformation of rat embryo cells on cellular oxygen consumption and glycolysis. Biochem Biophys Res Commun 1997;235:739-42.
34. Ramanathan A, Wang C, Schreiber SL. Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements. Proc Natl Acad Sci U S A 2005;102:5992-7.
35. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 2001;98:10869-74.
36. Buck A, Schirrmeister H, Kuhn T, Shen C, Kalker T, Kotzerke J, et al. FDG uptake in breast cancer: correlation with biological and clinical prognostic parameters. Eur J Nucl Med Mol Imaging 2002;29:1317-23.
37. Hanby AM, Hughes TA. In situ and invasive lobular neoplasia of the breast. Histopathology 2008;52:58-66.
38. Specht JM, Kurland BF, Montgomery SK, Dunnwald LK, Doot RK, Gralow JR, et al. Tumor metabolism and blood flow as assessed by positron emission tomography varies by tumor subtype in locally advanced breast cancer. Clin Cancer Res 2010;16:2803-10.
39. Basu S, Chen W, Tchou J, Mavi A, Cermik T, Czerniecki B, et al. Comparison of triple-negative and estrogen receptor-positive/progesterone receptor-positive/HER2-negative breast carcinoma using quantitative fluorine-18 fluorodeoxyglucose/positron emission tomography imaging parameters: a potentially useful method for disease characterization. Cancer 2008;112:995-1000.
40. Gunther EJ, Belka GK, Wertheim GB, Wang J, Hartman JL, Boxer RB, et al. A novel doxycycline-inducible system for the transgenic analysis of mammary gland biology. FASEB J 2002;16:283-92.
41. Boxer RB, Stairs DB, Dugan KD, Notarfrancesco KL, Portocarrero CP, Keister BA, et al. Isoform-specific requirement for Akt1 in the developmental regulation of cellular metabolism during lactation. Cell Metab 2006;4:475-90.
42. Boxer RB, Jang JW, Sintasath L, Chodosh LA. Lack of sustained regression of c-MYC-induced mammary adenocarcinomas following brief or prolonged MYC inactivation. Cancer Cell 2004;6:577-86.
43. Gunther EJ, Moody SE, Belka GK, Hahn KT, Innocent N, Dugan KD, et al. Impact of p53 loss on reversal and recurrence of conditional Wnt-induced tumorigenesis. Genes Dev 2003;17:488-501.
44. Moody SE, Sarkisian CJ, Hahn KT, Gunther EJ, Pickup S, Dugan KD, et al. Conditional activation of Neu in the mammary epithelium of transgenic mice results in reversible pulmonary metastasis. Cancer Cell 2002;2:451-61.
45. Sarkisian CJ, Keister BA, Stairs DB, Boxer RB, Moody SE, Chodosh LA. Dose-dependent oncogene-induced senescence in vivo and its evasion during mammary tumorigenesis. Nat Cell Biol 2007;9:493-505.
46. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, et al. Genes that mediate breast cancer metastasis to lung. Nature 2005;436:518-24.
47. Surti S, Karp JS, Perkins AE, Cardi CA, Daube-Witherspoon ME, Kuhn A, et al. Imaging performance of A-PET: a small animal PET camera. IEEE Trans Med Imaging 2005;24:844-52.
48. Surti S, Karp JS, Perkins AE, Freifelder R, Muehllehner G. Design evaluation of A-PET: a high sensitivity animal PET camera. IEEE Trans Nucl Sci 2003;50:1357-63.
49. Daube-Witherspoon M, Matej S, Karp J, Lewitt R. Application of the row action maximum likelihood algorithm with spherical basis functions to clinical PET imaging. IEEE Trans Nucl Sci 2001;48:24-30.
50. Zhao Y, Wieman HL, Jacobs SR, Rathmell JC. Mechanisms and methods in glucose metabolism and cell death. Methods Enzymol 2008;442:439-57.
51. Model F, Adorjan P, Olek A, Piepenbrock C. Feature selection for DNA methylation based cancer classification. Bioinformatics 2001;17:S157-64.
52. D'Cruz CM, Gunther EJ, Boxer RB, Hartman JL, Sintasath L, Moody SE, et al. c-MYC induces mammary tumorigenesis by means of a preferred pathway involving spontaneous Kras2 mutations. Nat Med 2001;7:235-9.
53. Ben-Haim S, Ell P. 18F-FDG PET and PET/CT in the evaluation of cancer treatment response. J Nucl Med 2009;50:88-99.
54. Bryant KL, Mancias JD, Kimmelman AC, Der CJ. KRAS: feeding pancreatic cancer proliferation. Trends Biochem Sci 2014;39:91-100.