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Published in: BMC Cancer 1/2017

Open Access 01-12-2017 | Research article

Non-invasively predicting differentiation of pancreatic cancer through comparative serum metabonomic profiling

Authors: Shi Wen, Bohan Zhan, Jianghua Feng, Weize Hu, Xianchao Lin, Jianxi Bai, Heguang Huang

Published in: BMC Cancer | Issue 1/2017

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Abstract

Background

The differentiation of pancreatic ductal adenocarcinoma (PDAC) could be associated with prognosis and may influence the choices of clinical management. No applicable methods could reliably predict the tumor differentiation preoperatively. Thus, the aim of this study was to compare the metabonomic profiling of pancreatic ductal adenocarcinoma with different differentiations and assess the feasibility of predicting tumor differentiations through metabonomic strategy based on nuclear magnetic resonance spectroscopy.

Methods

By implanting pancreatic cancer cell strains Panc-1, Bxpc-3 and SW1990 in nude mice in situ, we successfully established the orthotopic xenograft models of PDAC with different differentiations. The metabonomic profiling of serum from different PDAC was achieved and analyzed by using 1H nuclear magnetic resonance (NMR) spectroscopy combined with the multivariate statistical analysis. Then, the differential metabolites acquired were used for enrichment analysis of metabolic pathways to get a deep insight.

Results

An obvious metabonomic difference was demonstrated between all groups and the pattern recognition models were established successfully. The higher concentrations of amino acids, glycolytic and glutaminolytic participators in SW1990 and choline-contain metabolites in Panc-1 relative to other PDAC cells were demonstrated, which may be served as potential indicators for tumor differentiation. The metabolic pathways and differential metabolites identified in current study may be associated with specific pathways such as serine-glycine-one-carbon and glutaminolytic pathways, which can regulate tumorous proliferation and epigenetic regulation.

Conclusion

The NMR-based metabonomic strategy may be served as a non-invasive detection method for predicting tumor differentiation preoperatively.
Literature
1.
2.
go back to reference Sohn T, Yeo C, Lillemoe K, Koniaris L, Kaushal S, Sauter P, Coleman J, Hruban R, Cameron J. Resected adenocarcinoma of the pancreas - 616 patients: results, outcome and prognostic indicators. Gastroenterology. 2000;118(4):A1059.CrossRef Sohn T, Yeo C, Lillemoe K, Koniaris L, Kaushal S, Sauter P, Coleman J, Hruban R, Cameron J. Resected adenocarcinoma of the pancreas - 616 patients: results, outcome and prognostic indicators. Gastroenterology. 2000;118(4):A1059.CrossRef
3.
go back to reference Winter J, Cameron J, Campbell K, Chang D, Coleman J, Hodgin M, Sauter P, Hruban R, Riall T, Schulick R. 1423 Pancreaticoduodenectomies for pancreatic cancer: a single-institution experience. J Gastrointest Surg. 2006;10(9):1199–211.CrossRefPubMed Winter J, Cameron J, Campbell K, Chang D, Coleman J, Hodgin M, Sauter P, Hruban R, Riall T, Schulick R. 1423 Pancreaticoduodenectomies for pancreatic cancer: a single-institution experience. J Gastrointest Surg. 2006;10(9):1199–211.CrossRefPubMed
4.
go back to reference Makowiec F, Riediger H, Fischer E, Keck T, Opitz OG, Adam U, Hopt UT. M1547 the lymph node-ratio is the strongest factor predicting survival after resection of pancreatic cancer. Gastroenterology. 2008;134(4):A-870. Makowiec F, Riediger H, Fischer E, Keck T, Opitz OG, Adam U, Hopt UT. M1547 the lymph node-ratio is the strongest factor predicting survival after resection of pancreatic cancer. Gastroenterology. 2008;134(4):A-870.
5.
go back to reference Nagai S, Fujii T, Kodera Y, Kanda M, Sahin TT, Kanzaki A, Yamada S, Sugimoto H, Nomoto S, Takeda S. Impact of operative blood loss on survival in invasive Ductal Adenocarcinoma of the pancreas. Pancreas. 2010;40(1):3–9.CrossRef Nagai S, Fujii T, Kodera Y, Kanda M, Sahin TT, Kanzaki A, Yamada S, Sugimoto H, Nomoto S, Takeda S. Impact of operative blood loss on survival in invasive Ductal Adenocarcinoma of the pancreas. Pancreas. 2010;40(1):3–9.CrossRef
6.
go back to reference Shimada K, Sano T, Sakamoto Y, Kosuge T. Clinical implications of combined portal vein resection as a palliative procedure in patients undergoing pancreaticoduodenectomy for pancreatic head carcinoma. Ann Surg Oncol. 2006;13(12):1569–78.CrossRefPubMed Shimada K, Sano T, Sakamoto Y, Kosuge T. Clinical implications of combined portal vein resection as a palliative procedure in patients undergoing pancreaticoduodenectomy for pancreatic head carcinoma. Ann Surg Oncol. 2006;13(12):1569–78.CrossRefPubMed
7.
go back to reference Mitsuro K, Tsutomu F, Sahin TT, Akiyuki K, Shunji N, Suguru Y, Hiroyuki S, Shuji N, Shin T, Yasuhiro K. Invasion of the splenic artery is a crucial prognostic factor in carcinoma of the body and tail of the pancreas. Ann Surg. 2010;251(3):483–7.CrossRef Mitsuro K, Tsutomu F, Sahin TT, Akiyuki K, Shunji N, Suguru Y, Hiroyuki S, Shuji N, Shin T, Yasuhiro K. Invasion of the splenic artery is a crucial prognostic factor in carcinoma of the body and tail of the pancreas. Ann Surg. 2010;251(3):483–7.CrossRef
8.
go back to reference Sugiura T, Uesaka K, Mihara K, Sasaki K, Kanemoto H, Mizuno T, Okamura Y. Margin status, recurrence pattern, and prognosis after resection of pancreatic cancer. Surgery. 2013;154(5):1078–86.CrossRefPubMed Sugiura T, Uesaka K, Mihara K, Sasaki K, Kanemoto H, Mizuno T, Okamura Y. Margin status, recurrence pattern, and prognosis after resection of pancreatic cancer. Surgery. 2013;154(5):1078–86.CrossRefPubMed
9.
go back to reference Neoptolemos JP, Stocken DD, Dunn JA, Almond J, Beger HG, Pederzoli P, Bassi C, Dervenis C, Fernandez-Cruz L, Lacaine F, et al. Influence of resection margins on survival for patients with pancreatic cancer treated by adjuvant chemoradiation and/or chemotherapy in the ESPAC-1 randomized controlled trial. Ann Surg. 2001;234(6):758–68.CrossRefPubMedPubMedCentral Neoptolemos JP, Stocken DD, Dunn JA, Almond J, Beger HG, Pederzoli P, Bassi C, Dervenis C, Fernandez-Cruz L, Lacaine F, et al. Influence of resection margins on survival for patients with pancreatic cancer treated by adjuvant chemoradiation and/or chemotherapy in the ESPAC-1 randomized controlled trial. Ann Surg. 2001;234(6):758–68.CrossRefPubMedPubMedCentral
10.
go back to reference Saukkonen K, Hagstrom J, Mustonen H, Juuti A, Nordling S, Kallio P, Alitalo K, Seppanen H, Haglund C. PROX1 and beta-catenin are prognostic markers in pancreatic ductal adenocarcinoma. BMC Cancer. 2016;16:472.CrossRefPubMedPubMedCentral Saukkonen K, Hagstrom J, Mustonen H, Juuti A, Nordling S, Kallio P, Alitalo K, Seppanen H, Haglund C. PROX1 and beta-catenin are prognostic markers in pancreatic ductal adenocarcinoma. BMC Cancer. 2016;16:472.CrossRefPubMedPubMedCentral
11.
go back to reference Reiser-Erkan C, Erkan M, Pan Z, Bekasi S, Giese NA, Streit S, Michalski CW, Friess H, Kleeff J. Hypoxia-inducible proto-oncogene Pim-1 is a prognostic marker in pancreatic ductal adenocarcinoma. Cancer Biol Ther. 2008;7(9):1352–9.CrossRefPubMed Reiser-Erkan C, Erkan M, Pan Z, Bekasi S, Giese NA, Streit S, Michalski CW, Friess H, Kleeff J. Hypoxia-inducible proto-oncogene Pim-1 is a prognostic marker in pancreatic ductal adenocarcinoma. Cancer Biol Ther. 2008;7(9):1352–9.CrossRefPubMed
12.
go back to reference Neoptolemos JP, Stocken DD, Friess H, Bassi C, Dunn JA, Hickey H, Beger H, Fernandez-Cruz L, Dervenis C, Lacaine F, et al. A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med. 2004;350(12):1200–10.CrossRefPubMed Neoptolemos JP, Stocken DD, Friess H, Bassi C, Dunn JA, Hickey H, Beger H, Fernandez-Cruz L, Dervenis C, Lacaine F, et al. A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med. 2004;350(12):1200–10.CrossRefPubMed
13.
go back to reference Barugola G, Partelli S, Marcucci S, Sartori N, Capelli P, Bassi C, Pederzoli P, Falconi M. Resectable pancreatic cancer: who really benefits from resection? Ann Surg Oncol. 2009;16(12):3316–22.CrossRefPubMed Barugola G, Partelli S, Marcucci S, Sartori N, Capelli P, Bassi C, Pederzoli P, Falconi M. Resectable pancreatic cancer: who really benefits from resection? Ann Surg Oncol. 2009;16(12):3316–22.CrossRefPubMed
14.
go back to reference Hsu CC, Wolfgang CL, Laheru DA, Pawlik TM, Swartz MJ, Winter JM, Robinson R, Edil BH, Narang AK, Choti MA, et al. Early mortality risk score: identification of poor outcomes following upfront surgery for resectable pancreatic cancer. J Gastrointest Surg. 2012;16(4):753–61.CrossRefPubMedPubMedCentral Hsu CC, Wolfgang CL, Laheru DA, Pawlik TM, Swartz MJ, Winter JM, Robinson R, Edil BH, Narang AK, Choti MA, et al. Early mortality risk score: identification of poor outcomes following upfront surgery for resectable pancreatic cancer. J Gastrointest Surg. 2012;16(4):753–61.CrossRefPubMedPubMedCentral
15.
go back to reference Joliat GR, Petermann D, Demartines N, Schafer M. External assessment of the early mortality risk score in patients with adenocarcinoma undergoing pancreaticoduodenectomy. HPB (Oxford). 2015;17(7):605–10.CrossRef Joliat GR, Petermann D, Demartines N, Schafer M. External assessment of the early mortality risk score in patients with adenocarcinoma undergoing pancreaticoduodenectomy. HPB (Oxford). 2015;17(7):605–10.CrossRef
16.
go back to reference Mornex F, Girard N, Delpero JR, Partensky C. Radiochemotherapy in the management of pancreatic cancer--part I: neoadjuvant treatment. Semin Radiat Oncol. 2005;15(4):226–34.CrossRefPubMed Mornex F, Girard N, Delpero JR, Partensky C. Radiochemotherapy in the management of pancreatic cancer--part I: neoadjuvant treatment. Semin Radiat Oncol. 2005;15(4):226–34.CrossRefPubMed
17.
go back to reference Quiros RM, Brown KM, Hoffman JP. Neoadjuvant therapy in pancreatic cancer. Cancer Investig. 2007;25(4):267–73.CrossRef Quiros RM, Brown KM, Hoffman JP. Neoadjuvant therapy in pancreatic cancer. Cancer Investig. 2007;25(4):267–73.CrossRef
18.
go back to reference Varadhachary GR, Tamm EP, Abbruzzese JL, Xiong HQ, Crane CH, Wang H, Lee JE, Pisters PW, Evans DB, Wolff RA. Borderline resectable pancreatic cancer: definitions, management, and role of preoperative therapy. Ann Surg Oncol. 2006;13(8):1035–46.CrossRefPubMed Varadhachary GR, Tamm EP, Abbruzzese JL, Xiong HQ, Crane CH, Wang H, Lee JE, Pisters PW, Evans DB, Wolff RA. Borderline resectable pancreatic cancer: definitions, management, and role of preoperative therapy. Ann Surg Oncol. 2006;13(8):1035–46.CrossRefPubMed
19.
go back to reference Larghi A, Correale L, Ricci R, Abdulkader I, Monges G, Iglesias-Garcia J, Giovannini M, Attili F, Vitale G, Hassan C, et al. Interobserver agreement and accuracy of preoperative endoscopic ultrasound-guided biopsy for histological grading of pancreatic cancer. Endoscopy. 2015;47(4):308–14.PubMed Larghi A, Correale L, Ricci R, Abdulkader I, Monges G, Iglesias-Garcia J, Giovannini M, Attili F, Vitale G, Hassan C, et al. Interobserver agreement and accuracy of preoperative endoscopic ultrasound-guided biopsy for histological grading of pancreatic cancer. Endoscopy. 2015;47(4):308–14.PubMed
20.
go back to reference Nurmi A, Haglund C, Mustonen H, Seppänen H. Neoadjuvant therapy offers longer survival for pancreatic cancer patients over upfront surgery. Pancreatology. 2017;17(3):S73.CrossRef Nurmi A, Haglund C, Mustonen H, Seppänen H. Neoadjuvant therapy offers longer survival for pancreatic cancer patients over upfront surgery. Pancreatology. 2017;17(3):S73.CrossRef
21.
go back to reference Mokdad AA, Minter RM, Zhu H, Augustine MM, Porembka MR, Wang SC, Yopp AC, Mansour JC, Choti MA, Polanco PM. Neoadjuvant therapy followed by resection versus upfront resection for Resectable pancreatic cancer: a propensity score matched analysis. J Clin Oncol. 2016;35(4):515-22. Mokdad AA, Minter RM, Zhu H, Augustine MM, Porembka MR, Wang SC, Yopp AC, Mansour JC, Choti MA, Polanco PM. Neoadjuvant therapy followed by resection versus upfront resection for Resectable pancreatic cancer: a propensity score matched analysis. J Clin Oncol. 2016;35(4):515-22.
23.
go back to reference Farrell JM, Pang JC, Kim GE, Tabatabai ZL. Pancreatic neuroendocrine tumors: accurate grading with Ki-67 index on fine-needle aspiration specimens using the WHO 2010/ENETS criteria. Cancer Cytopathol. 2014;122(10):770–8.CrossRefPubMed Farrell JM, Pang JC, Kim GE, Tabatabai ZL. Pancreatic neuroendocrine tumors: accurate grading with Ki-67 index on fine-needle aspiration specimens using the WHO 2010/ENETS criteria. Cancer Cytopathol. 2014;122(10):770–8.CrossRefPubMed
24.
go back to reference Pitman MB, Centeno BA, Genevay M, Fonseca R, Mino-Kenudson M. Grading epithelial atypia in endoscopic ultrasound-guided fine-needle aspiration of intraductal papillary mucinous neoplasms: an international interobserver concordance study. Cancer Cytopathol. 2013;121(12):729–36.CrossRefPubMed Pitman MB, Centeno BA, Genevay M, Fonseca R, Mino-Kenudson M. Grading epithelial atypia in endoscopic ultrasound-guided fine-needle aspiration of intraductal papillary mucinous neoplasms: an international interobserver concordance study. Cancer Cytopathol. 2013;121(12):729–36.CrossRefPubMed
25.
go back to reference Brindle JT, Antti H, Holmes E, Tranter G, Nicholson JK, Bethell HWL, Clarke S, Schofield PM, Mckilligin E, Mosedale DE. Rapid and noninvasive diagnosis of the presence and severity of coronary heart disease using 1H-NMR-based metabonomics. Nat Med. 2002;8(12):1439–44.CrossRefPubMed Brindle JT, Antti H, Holmes E, Tranter G, Nicholson JK, Bethell HWL, Clarke S, Schofield PM, Mckilligin E, Mosedale DE. Rapid and noninvasive diagnosis of the presence and severity of coronary heart disease using 1H-NMR-based metabonomics. Nat Med. 2002;8(12):1439–44.CrossRefPubMed
26.
go back to reference Bartella L, Morris EA, Dershaw DD, Liberman L, Thakur SB, Moskowitz C, Guido J, Huang W. Proton MR spectroscopy with choline peak as malignancy marker improves positive predictive value for breast cancer diagnosis: preliminary study. Radiology. 2006;239(3):686–92.CrossRefPubMed Bartella L, Morris EA, Dershaw DD, Liberman L, Thakur SB, Moskowitz C, Guido J, Huang W. Proton MR spectroscopy with choline peak as malignancy marker improves positive predictive value for breast cancer diagnosis: preliminary study. Radiology. 2006;239(3):686–92.CrossRefPubMed
27.
go back to reference Huzjan R, Sala E, Hricak H. Magnetic resonance imaging and magnetic resonance spectroscopic imaging of prostate cancer. Nat Clin Pract Urol. 2005;2(9):434–42.CrossRefPubMed Huzjan R, Sala E, Hricak H. Magnetic resonance imaging and magnetic resonance spectroscopic imaging of prostate cancer. Nat Clin Pract Urol. 2005;2(9):434–42.CrossRefPubMed
28.
go back to reference Khan SA, Cox IJ, Thillainayagam AV, Bansi DS, Thomas HC, Taylor-Robinson SD. Proton and phosphorus-31 nuclear magnetic resonance spectroscopy of human bile in hepatopancreaticobiliary cancer. Eur J Gastroenterol Hepatol. 2005;17(7):733–8.CrossRefPubMed Khan SA, Cox IJ, Thillainayagam AV, Bansi DS, Thomas HC, Taylor-Robinson SD. Proton and phosphorus-31 nuclear magnetic resonance spectroscopy of human bile in hepatopancreaticobiliary cancer. Eur J Gastroenterol Hepatol. 2005;17(7):733–8.CrossRefPubMed
29.
go back to reference Kwock L, Smith JK, Castillo M, Ewend MG, Collichio F, Morris DE, Bouldin TW, Cush S. Clinical role of proton magnetic resonance spectroscopy in oncology: brain, breast, and prostate cancer. Lancet Oncol. 2006;7(10):859–68.CrossRefPubMed Kwock L, Smith JK, Castillo M, Ewend MG, Collichio F, Morris DE, Bouldin TW, Cush S. Clinical role of proton magnetic resonance spectroscopy in oncology: brain, breast, and prostate cancer. Lancet Oncol. 2006;7(10):859–68.CrossRefPubMed
30.
go back to reference Rehman L, Rehman UL, Azmat SK, Mohammad Hashim AS. Magnetic resonance spectroscopy: novel non-invasive technique for diagnosing brain tumors. J Coll Physicians Surg Pak. 2015;25(12):863–6.PubMed Rehman L, Rehman UL, Azmat SK, Mohammad Hashim AS. Magnetic resonance spectroscopy: novel non-invasive technique for diagnosing brain tumors. J Coll Physicians Surg Pak. 2015;25(12):863–6.PubMed
31.
go back to reference Thomas MA, Wyckoff N, Yue K, Binesh N, Banakar S, Chung HK, Sayre J, DeBruhl N. Two-dimensional MR spectroscopic characterization of breast cancer in vivo. Technol Cancer Res Treat. 2005;4(1):99–106.CrossRefPubMed Thomas MA, Wyckoff N, Yue K, Binesh N, Banakar S, Chung HK, Sayre J, DeBruhl N. Two-dimensional MR spectroscopic characterization of breast cancer in vivo. Technol Cancer Res Treat. 2005;4(1):99–106.CrossRefPubMed
32.
go back to reference Kaplan O, Kushnir T, Askenazy N, Knubovets T, Navon G. Role of nuclear magnetic resonance spectroscopy (MRS) in cancer diagnosis and treatment: 31P, 23Na, and 1H MRS studies of three models of pancreatic cancer. Cancer Res. 1997;57(8):1452–9.PubMed Kaplan O, Kushnir T, Askenazy N, Knubovets T, Navon G. Role of nuclear magnetic resonance spectroscopy (MRS) in cancer diagnosis and treatment: 31P, 23Na, and 1H MRS studies of three models of pancreatic cancer. Cancer Res. 1997;57(8):1452–9.PubMed
33.
go back to reference Bathe OF, Shaykhutdinov R, Kopciuk K, Weljie AM, McKay A, Sutherland FR, Dixon E, Dunse N, Sotiropoulos D, Vogel HJ. Feasibility of identifying pancreatic cancer based on serum metabolomics. Cancer Epidemiol Biomarkers Prev. 2011;20(1):140–7.CrossRefPubMed Bathe OF, Shaykhutdinov R, Kopciuk K, Weljie AM, McKay A, Sutherland FR, Dixon E, Dunse N, Sotiropoulos D, Vogel HJ. Feasibility of identifying pancreatic cancer based on serum metabolomics. Cancer Epidemiol Biomarkers Prev. 2011;20(1):140–7.CrossRefPubMed
34.
go back to reference Zhang L, Jin H, Guo X, Yang Z, Zhao L, Tang S, Mo P, Wu K, Nie Y, Pan Y, et al. Distinguishing pancreatic cancer from chronic pancreatitis and healthy individuals by (1)H nuclear magnetic resonance-based metabonomic profiles. Clin Biochem. 2012;45(13-14):1064–9.CrossRefPubMed Zhang L, Jin H, Guo X, Yang Z, Zhao L, Tang S, Mo P, Wu K, Nie Y, Pan Y, et al. Distinguishing pancreatic cancer from chronic pancreatitis and healthy individuals by (1)H nuclear magnetic resonance-based metabonomic profiles. Clin Biochem. 2012;45(13-14):1064–9.CrossRefPubMed
35.
go back to reference Fang F, He X, Deng H, Chen Q, Lu J, Spraul M, Yu Y. Discrimination of metabolic profiles of pancreatic cancer from chronic pancreatitis by high-resolution magic angle spinning 1H nuclear magnetic resonance and principal components analysis. Cancer Sci. 2007;98(11):1678–82.CrossRefPubMed Fang F, He X, Deng H, Chen Q, Lu J, Spraul M, Yu Y. Discrimination of metabolic profiles of pancreatic cancer from chronic pancreatitis by high-resolution magic angle spinning 1H nuclear magnetic resonance and principal components analysis. Cancer Sci. 2007;98(11):1678–82.CrossRefPubMed
36.
go back to reference Tan MH, Nowak NJ, Loor R, ., Ochi H, ., Sandberg AA, Lopez C, ., Pickren JW, Berjian R, ., Douglass HO, Chu TM: Characterization of a new primary human pancreatic tumor line. Cancer Investig 1986, 4(1):15-23.CrossRef Tan MH, Nowak NJ, Loor R, ., Ochi H, ., Sandberg AA, Lopez C, ., Pickren JW, Berjian R, ., Douglass HO, Chu TM: Characterization of a new primary human pancreatic tumor line. Cancer Investig 1986, 4(1):15-23.CrossRef
37.
go back to reference Kyriazis AP, Sandberg AA, Kyriazis AA, Sloane NH, Lepera R. Establishment and characterization of human pancreatic adenocarcinoma cell line SW-1990 in tissue culture and the nude mouse. Cancer Res. 1983;43(9):4393–401.PubMed Kyriazis AP, Sandberg AA, Kyriazis AA, Sloane NH, Lepera R. Establishment and characterization of human pancreatic adenocarcinoma cell line SW-1990 in tissue culture and the nude mouse. Cancer Res. 1983;43(9):4393–401.PubMed
38.
go back to reference Lieber M, ., Mazzetta J, ., Nelson-Rees W, ., Kaplan M, ., Todaro G,. Establishment of a continuous tumor-cell line (panc-1) from a human carcinoma of the exocrine pancreas. Int J Cancer 1975, 15(5):741-747.CrossRefPubMed Lieber M, ., Mazzetta J, ., Nelson-Rees W, ., Kaplan M, ., Todaro G,. Establishment of a continuous tumor-cell line (panc-1) from a human carcinoma of the exocrine pancreas. Int J Cancer 1975, 15(5):741-747.CrossRefPubMed
39.
go back to reference Deer EL, Jessica GH, Coursen JD, Shea JE, Josephat N, Scaife CL, Firpo MA, Mulvihill SJ. Phenotype and genotype of pancreatic cancer cell lines. Pancreas. 2010;39(4):425–35.CrossRefPubMedPubMedCentral Deer EL, Jessica GH, Coursen JD, Shea JE, Josephat N, Scaife CL, Firpo MA, Mulvihill SJ. Phenotype and genotype of pancreatic cancer cell lines. Pancreas. 2010;39(4):425–35.CrossRefPubMedPubMedCentral
40.
go back to reference Chagoyen M, Pazos F. MBRole: enrichment analysis of metabolomic data. Bioinformatics. 2011;27(5):730–1.CrossRefPubMed Chagoyen M, Pazos F. MBRole: enrichment analysis of metabolomic data. Bioinformatics. 2011;27(5):730–1.CrossRefPubMed
41.
go back to reference Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42(Database issue):D199–205.CrossRefPubMed Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42(Database issue):D199–205.CrossRefPubMed
42.
go back to reference Wishart DS, Knox C, Guo AC, Eisner R, Young N, Gautam B, Hau DD, Psychogios N, Dong E, Bouatra S, et al. HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res. 2009;37(Database issue):D603–10.CrossRefPubMed Wishart DS, Knox C, Guo AC, Eisner R, Young N, Gautam B, Hau DD, Psychogios N, Dong E, Bouatra S, et al. HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res. 2009;37(Database issue):D603–10.CrossRefPubMed
43.
go back to reference Cui Q, Lewis IA, Hegeman AD, Anderson ME, Li J, Schulte CF, Westler WM, Eghbalnia HR, Sussman MR, Markley JL. Metabolite identification via the Madison Metabolomics consortium database. Nat Biotechnol. 2008;26(2):162–4.CrossRefPubMed Cui Q, Lewis IA, Hegeman AD, Anderson ME, Li J, Schulte CF, Westler WM, Eghbalnia HR, Sussman MR, Markley JL. Metabolite identification via the Madison Metabolomics consortium database. Nat Biotechnol. 2008;26(2):162–4.CrossRefPubMed
44.
go back to reference Hirschhaeuser F, Sattler UG, Mueller-Klieser W. Lactate: a metabolic key player in cancer. Cancer Res. 2011;71(22):6921–5.CrossRefPubMed Hirschhaeuser F, Sattler UG, Mueller-Klieser W. Lactate: a metabolic key player in cancer. Cancer Res. 2011;71(22):6921–5.CrossRefPubMed
45.
go back to reference Guillaumond F, Leca J, Olivares O, Lavaut MN, Vidal N, Berthezene P, Dusetti NJ, Loncle C, Calvo E, Turrini O, et al. Strengthened glycolysis under hypoxia supports tumor symbiosis and hexosamine biosynthesis in pancreatic adenocarcinoma. Proc Natl Acad Sci U S A. 2013;110(10):3919–24.CrossRefPubMedPubMedCentral Guillaumond F, Leca J, Olivares O, Lavaut MN, Vidal N, Berthezene P, Dusetti NJ, Loncle C, Calvo E, Turrini O, et al. Strengthened glycolysis under hypoxia supports tumor symbiosis and hexosamine biosynthesis in pancreatic adenocarcinoma. Proc Natl Acad Sci U S A. 2013;110(10):3919–24.CrossRefPubMedPubMedCentral
46.
go back to reference OuYang D, Xu J, Huang H, Chen Z. Metabolomic profiling of serum from human pancreatic cancer patients using 1H NMR spectroscopy and principal component analysis. Appl Biochem Biotechnol. 2011;165(1):148–54.CrossRefPubMed OuYang D, Xu J, Huang H, Chen Z. Metabolomic profiling of serum from human pancreatic cancer patients using 1H NMR spectroscopy and principal component analysis. Appl Biochem Biotechnol. 2011;165(1):148–54.CrossRefPubMed
47.
go back to reference Kobayashi T, Nishiumi S, Ikeda A, Yoshie T, Sakai A, Matsubara A, Izumi Y, Tsumura H, Tsuda M, Nishisaki H, et al. A novel serum metabolomics-based diagnostic approach to pancreatic cancer. Cancer Epidemiol Biomarkers Prev. 2013;22(4):571–9.CrossRefPubMed Kobayashi T, Nishiumi S, Ikeda A, Yoshie T, Sakai A, Matsubara A, Izumi Y, Tsumura H, Tsuda M, Nishisaki H, et al. A novel serum metabolomics-based diagnostic approach to pancreatic cancer. Cancer Epidemiol Biomarkers Prev. 2013;22(4):571–9.CrossRefPubMed
48.
go back to reference Soga T. Cancer metabolism: key players in metabolic reprogramming. Cancer Sci. 2013;104(3):275–81.CrossRefPubMed Soga T. Cancer metabolism: key players in metabolic reprogramming. Cancer Sci. 2013;104(3):275–81.CrossRefPubMed
49.
go back to reference Son J, Lyssiotis CA, Ying H, Wang X, Hua S, Ligorio M, Perera RM, Ferrone CR, Mullarky E, Shyh-Chang N, et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature. 2013;496(7443):101–5.CrossRefPubMedPubMedCentral Son J, Lyssiotis CA, Ying H, Wang X, Hua S, Ligorio M, Perera RM, Ferrone CR, Mullarky E, Shyh-Chang N, et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature. 2013;496(7443):101–5.CrossRefPubMedPubMedCentral
50.
go back to reference Mayers JR, Wu C, Clish CB, Kraft P, Torrence ME, Fiske BP, Yuan C, Bao Y, Townsend MK, Tworoger SS, et al. Elevation of circulating branched-chain amino acids is an early event in human pancreatic adenocarcinoma development. Nat Med. 2014;20(10):1193–8.CrossRefPubMedPubMedCentral Mayers JR, Wu C, Clish CB, Kraft P, Torrence ME, Fiske BP, Yuan C, Bao Y, Townsend MK, Tworoger SS, et al. Elevation of circulating branched-chain amino acids is an early event in human pancreatic adenocarcinoma development. Nat Med. 2014;20(10):1193–8.CrossRefPubMedPubMedCentral
51.
go back to reference Fuchs BC, Bode BP. Amino acid transporters ASCT2 and LAT1 in cancer: partners in crime? Semin Cancer Biol. 2005;15(4):254–66.CrossRefPubMed Fuchs BC, Bode BP. Amino acid transporters ASCT2 and LAT1 in cancer: partners in crime? Semin Cancer Biol. 2005;15(4):254–66.CrossRefPubMed
52.
go back to reference Kaira K, Sunose Y, Arakawa K, Ogawa T, Sunaga N, Shimizu K, Tominaga H, Oriuchi N, Itoh H, Nagamori S, et al. Prognostic significance of L-type amino-acid transporter 1 expression in surgically resected pancreatic cancer. Br J Cancer. 2012;107(4):632–8.CrossRefPubMedPubMedCentral Kaira K, Sunose Y, Arakawa K, Ogawa T, Sunaga N, Shimizu K, Tominaga H, Oriuchi N, Itoh H, Nagamori S, et al. Prognostic significance of L-type amino-acid transporter 1 expression in surgically resected pancreatic cancer. Br J Cancer. 2012;107(4):632–8.CrossRefPubMedPubMedCentral
54.
go back to reference Tedeschi PM, Markert EK, Gounder M, Lin H, Dvorzhinski D, Dolfi SC, Chan LL, Qiu J, DiPaola RS, Hirshfield KM, et al. Contribution of serine, folate and glycine metabolism to the ATP, NADPH and purine requirements of cancer cells. Cell Death Dis. 2013;4:e877.CrossRefPubMedPubMedCentral Tedeschi PM, Markert EK, Gounder M, Lin H, Dvorzhinski D, Dolfi SC, Chan LL, Qiu J, DiPaola RS, Hirshfield KM, et al. Contribution of serine, folate and glycine metabolism to the ATP, NADPH and purine requirements of cancer cells. Cell Death Dis. 2013;4:e877.CrossRefPubMedPubMedCentral
55.
go back to reference Kottakis F, Nicolay BN, Roumane A, Karnik R, Gu H, Nagle JM, Boukhali M, Hayward MC, Li YY, Chen T, et al. LKB1 loss links serine metabolism to DNA methylation and tumorigenesis. Nature. 2016;539(7629):390-95. Kottakis F, Nicolay BN, Roumane A, Karnik R, Gu H, Nagle JM, Boukhali M, Hayward MC, Li YY, Chen T, et al. LKB1 loss links serine metabolism to DNA methylation and tumorigenesis. Nature. 2016;539(7629):390-95.
56.
go back to reference Glunde K, Bhujwalla ZM, Ronen SM. Choline metabolism in malignant transformation. Nat Rev Cancer. 2011;11(12):835–48.PubMedPubMedCentral Glunde K, Bhujwalla ZM, Ronen SM. Choline metabolism in malignant transformation. Nat Rev Cancer. 2011;11(12):835–48.PubMedPubMedCentral
57.
go back to reference Stewart JD, Marchan R, Lesjak MS, Lambert J, Hergenroeder R, Ellis JK, Lau CH, Keun HC, Schmitz G, Schiller J, et al. Choline-releasing glycerophosphodiesterase EDI3 drives tumor cell migration and metastasis. Proc Natl Acad Sci U S A. 2012;109(21):8155–60.CrossRefPubMedPubMedCentral Stewart JD, Marchan R, Lesjak MS, Lambert J, Hergenroeder R, Ellis JK, Lau CH, Keun HC, Schmitz G, Schiller J, et al. Choline-releasing glycerophosphodiesterase EDI3 drives tumor cell migration and metastasis. Proc Natl Acad Sci U S A. 2012;109(21):8155–60.CrossRefPubMedPubMedCentral
58.
go back to reference Penet MF, Shah T, Bharti S, Krishnamachary B, Artemov D, Mironchik Y, Wildes F, Maitra A, Bhujwalla ZM. Metabolic imaging of pancreatic ductal adenocarcinoma detects altered choline metabolism. Clin Cancer Res. 2015;21(2):386–95.CrossRefPubMed Penet MF, Shah T, Bharti S, Krishnamachary B, Artemov D, Mironchik Y, Wildes F, Maitra A, Bhujwalla ZM. Metabolic imaging of pancreatic ductal adenocarcinoma detects altered choline metabolism. Clin Cancer Res. 2015;21(2):386–95.CrossRefPubMed
Metadata
Title
Non-invasively predicting differentiation of pancreatic cancer through comparative serum metabonomic profiling
Authors
Shi Wen
Bohan Zhan
Jianghua Feng
Weize Hu
Xianchao Lin
Jianxi Bai
Heguang Huang
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2017
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-017-3703-9

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