Role of CPS1 in cell growth, metabolism, and prognosis in LKB1-inactivated lung adenocarcinoma

Journal of the National Cancer Institute

Volumn 109, Issue 3, 2017, Pages

  Celiktas, Muge ^a   Tanaka, Ichidai ^a   Tripathi, Satyendra Chandra ^a   Fahrmann, Johannes F ^a   Aguilar Bonavides, Clemente ^a   Villalobos, Pamela ^a   Delgado, Oliver ^a   Dhillon, Dilsher ^a   Dennison, Jennifer B ^a   Ostrin, Edwin J ^a   Wang, Hong ^a   Behrens, Carmen ^a   Do, Kim Anh ^a   Gazdar, Adi F ^b   Hanash, Samir M ^a   Taguchi, Ayumu ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 (3 FLUOROPHENYL) N (3 PIPERIDINYL) 3 UREIDO 2 THIOPHENECARBOXAMIDE; CARBAMOYL PHOSPHATE SYNTHASE; GEMCITABINE; PEMETREXED; PROTEIN KINASE LKB1; PROTEOME; 3-(CARBAMOYLAMINO)-5-(3-FLUOROPHENYL)-N-(3-PIPERIDYL)THIOPHENE-2-CARBOXAMIDE; DEOXYCYTIDINE; MESSENGER RNA; PROTEIN SERINE THREONINE KINASE; STK11 PROTEIN, HUMAN; THIOPHENE DERIVATIVE; UREA;

ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CELL GROWTH; CELL METABOLISM; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; MASS SPECTROMETRY; METABOLOME; MICROARRAY ANALYSIS; NUCLEIC ACID SYNTHESIS; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; TISSUE MICROARRAY; ADENOCARCINOMA; AGED; ANALOGS AND DERIVATIVES; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; FEMALE; GENE SILENCING; GENETICS; KAPLAN MEIER METHOD; LUNG TUMOR; MALE; METABOLISM; MIDDLE AGED; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; SURVIVAL RATE; TUMOR CELL LINE;

ADENOCARCINOMA; AGED; CARBAMOYL-PHOSPHATE SYNTHASE (AMMONIA); CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; DEOXYCYTIDINE; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MALE; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; MIDDLE AGED; PEMETREXED; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; PROTEIN-SERINE-THREONINE KINASES; PROTEOME; RNA, MESSENGER; SIGNAL TRANSDUCTION; SURVIVAL RATE; THIOPHENES; TISSUE ARRAY ANALYSIS; UREA;

EID: 85018160687     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djw231     Document Type: Article

References (53)

1. Sanchez-Cespedes M. A role for LKB1 gene in human cancer beyond the Peutz-Jeghers syndrome. Oncogene. 2007;26(57):7825-7832.
2. Cancer Genome Atlas Research Network. Comprehensive molecular profiling of lung adenocarcinoma. Nature. 2014;511(7511):543-550.
3. Ding L, Getz G, Wheeler DA, et al. Somatic mutations affect key pathways in lung adenocarcinoma. Nature. 2008;455(7216):1069-1075.
4. Govindan R, Ding L, Griffith M, et al. Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell. 2012;150(6):1121-1134.
5. Imielinski M, Berger AH, Hammerman PS, et al. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell. 2012;150(6): 1107-1120.
6. Matsumoto S, Iwakawa R, Takahashi K, et al. Prevalence and specificity of LKB1 genetic alterations in lung cancers. Oncogene. 2007;26(40):5911-5918.
7. Gill RK, Yang SH, Meerzaman D, et al. Frequent homozygous deletion of the LKB1/STK11 gene in non-small cell lung cancer. Oncogene. 2011;30(35):3784-3791.
8. Esteller M, Avizienyte E, Corn PG, et al. Epigenetic inactivation of LKB1 in primary tumors associated with the Peutz-Jeghers syndrome. Oncogene. 2000; 19(1):164-168.
9. Carretero J, Shimamura T, Rikova K, et al. Integrative genomic and proteomic analyses identify targets for Lkb1-deficient metastatic lung tumors. Cancer Cell. 2010;17(6):547-559.
10. Ji H, Ramsey MR, Hayes DN, et al. LKB1 modulates lung cancer differentiation and metastasis. Nature. 2007;448(7155):807-810.
11. Chen Z, Cheng K, Walton Z, et al. A murine lung cancer co-clinical trial identifies genetic modifiers of therapeutic response. Nature. 2012;483(7391): 613-617.
12. Gan RY, Li HB. Recent progress on liver kinase B1 (LKB1): Expression, regulation, downstream signaling and cancer suppressive function. Int J Mol Sci. 2014;15(9):16698-16718.
13. Alessi DR, Sakamoto K, Bayascas JR. LKB1-dependent signaling pathways. Annu Rev Biochem. 2006;75:137-163.
14. Chen Z, Fillmore CM, Hammerman PS, et al. Non-small-cell lung cancers: A heterogeneous set of diseases. Nat Rev Cancer. 2014;14(8):535-546.
15. Shah U, Sharpless NE, Hayes DN. LKB1 and lung cancer: More than the usual suspects. Cancer Res. 2008;68(10):3562-3565.
16. Summar ML, Dasouki MJ, Schofield PJ, et al. Physical and linkage mapping of human carbamyl phosphate synthetase I (CPS1) and reassignment from 2p to 2q35. Cytogenet Cell Genet. 1995;71(3):266-267.
17. Pausch J, Rasenack J, Haussinger D, et al. Hepatic carbamoyl phosphate metabolism. Role of cytosolic and mitochondrial carbamoyl phosphate in de novo pyrimidine synthesis. Eur J Biochem. 1985;150(1):189-194.
18. Levin B, Oberholzer VG, Sinclair L. Biochemical investigations of hyperammonaemia. Lancet. 1969;2(7613):170-174.
19. Morris SM Jr. Regulation of enzymes of the urea cycle and arginine metabolism. Annu Rev Nutr. 2002;22:87-105.
20. Taguchi A, Politi K, Pitteri SJ, et al. Lung cancer signatures in plasma based on proteome profiling of mouse tumor models. Cancer Cell. 2011;20(3):289-299.
21. Cox DR, Oakes D. Analysis of survival data. London and New York: Chapman and Hall; 1984.
22. Forbes SA, Beare D, Gunasekaran P, et al. COSMIC: Exploring the world's knowledge of somatic mutations in human cancer. Nucleic Acids Res. 2015; 43(Database issue):D805-D811.
23. Schliekelman MJ, Taguchi A, Zhu J, et al. Molecular portraits of epithelial, mesenchymal, and hybrid States in lung adenocarcinoma and their relevance to survival. Cancer Res. 2015;75(9):1789-1800.
24. Taguchi A, Delgado O, CeliktasM, et al. Proteomic signatures associatedwith p53 mutational status in lung adenocarcinoma. Proteomics. 2014;14(23-24):2750-2759.
25. Eng CH, Yu K, Lucas J, et al. Ammonia derived from glutaminolysis is a diffusible regulator of autophagy. Sci Signal. 2010;3(119):ra31.
26. Polletta L, Vernucci E, Carnevale I, et al. SIRT5 regulation of ammoniainduced autophagy and mitophagy. Autophagy. 2015;11(2):253-270.
27. Reck M, Heigener DF, Mok T, et al. Management of non-small-cell lung cancer: Recent developments. Lancet. 2013;382(9893):709-719.
28. Liu Y, Marks K, Cowley GS, et al. Metabolic and functional genomic studies identify deoxythymidylate kinase as a target in LKB1-mutant lung cancer. Cancer Discov. 2013;3(8):870-879.
29. Butler SL, Dong H, Cardona D, et al. The antigen for Hep Par 1 antibody is the urea cycle enzyme carbamoyl phosphate synthetase 1. Lab Invest. 2008;88(1):78-88.
30. Fan Z, van de Rijn M, Montgomery K, et al. Hep par 1 antibody stain for the differential diagnosis of hepatocellular carcinoma: 676 tumors tested using tissue microarrays and conventional tissue sections. Mod Pathol. 2003;16(2):137-144.
31. Liu H, Dong H, Robertson K, et al. DNA methylation suppresses expression of the urea cycle enzyme carbamoyl phosphate synthetase 1 (CPS1) in human hepatocellular carcinoma. Am J Pathol. 2011;178(2):652-661.
32. Siddiqui MT, Saboorian MH, Gokaslan ST, et al. Diagnostic utility of the HepPar1 antibody to differentiate hepatocellular carcinoma from metastatic carcinoma in fine-needle aspiration samples. Cancer. 2002;96(1):49-52.
33. Lee YY, Li CF, Lin CY, et al. Overexpression of CPS1 is an independent negative prognosticator in rectal cancers receiving concurrent chemoradiotherapy. Tumour Biol. 2014;35(11):11097-11105.
34. Sato T, Kashima K, Gamachi A, et al. Immunohistochemical localization of pyruvate carboxylase and carbamyl-phosphate synthetase I in normal and neoplastic human pancreatic tissues. Pancreas. 2002;25(2):130-135.
35. Chu PG, Weiss LM. Immunohistochemical characterization of signet-ring cell carcinomas of the stomach, breast, and colon. Am J Clin Pathol. 2004;121(6): 884-892.
36. Brentnall TA, Pan S, Bronner MP, et al. Proteins that underlie neoplastic progression of ulcerative colitis. Proteomics Clin Appl. 2009;3(11):1326.
37. Thamboo TP, Wee A. Hep Par 1 expression in carcinoma of the cervix: Implications for diagnosis and prognosis. J Clin Pathol. 2004;57(1):48-53.
38. Kaufman JM, Amann JM, Park K, et al. LKB1 loss induces characteristic patterns of gene expression in human tumors associated with NRF2 activation and attenuation of PI3K-AKT. J Thorac Oncol. 2014;9(6):794-804.
39. Skoulidis F, Byers LA, Diao L, et al. Co-occurring genomic alterations definemajor subsets of KRAS-mutant lung adenocarcinoma with distinct biology, immune profiles, and therapeutic vulnerabilities. Cancer Discov. 2015;5(8):860-877.
40. Chen YR, Sekine K, Nakamura K, et al. Y-box binding protein-1 down-regulates expression of carbamoyl phosphate synthetase-I by suppressing CCAAT enhancer-binding protein-alpha function in mice. Gastroenterology. 2009;137(1):330-340.
41. Christoffels VM, van den Hoff MJ, Moorman AF, et al. The far-upstream enhancer of the carbamoyl-phosphate synthetase I gene is responsible for the tissue specificity and hormone inducibility of its expression. J Biol Chem. 1995; 270(42):24932-24940.
42. Lagace M, Goping IS, Mueller CR, et al. The carbamyl phosphate synthetase promoter contains multiple binding sites for C/EBP-related proteins. Gene. 1992;118(2):231-238.
43. Nakagawa T, Lomb DJ, Haigis MC, et al. SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell. 2009;137(3):560-570.
44. Du J, Zhou Y, Su X, et al. Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science. 2011;334(6057):806-809.
45. Buler M, Aatsinki SM, Izzi V, et al. SIRT5 is under the control of PGC-1alpha and AMPK and is involved in regulation of mitochondrial energy metabolism. FASEB J. 2014;28(7):3225-3237.
46. Shackelford DB, Abt E, Gerken L, et al. LKB1 inactivation dictates therapeutic response of non-small cell lung cancer to the metabolism drug phenformin. Cancer Cell. 2013;23(2):143-158.
47. Mukhopadhyay A, Berrett KC, Kc U, et al. Sox2 cooperates with Lkb1 loss in a mouse model of squamous cell lung cancer. Cell Rep. 2014;8(1):40-49.
48. Koyama S, Akbay EA, Li YY, et al. STK11/LKB1 deficiency promotes neutrophil recruitment and proinflammatory cytokine production to suppress t-cell activity in the lung tumor microenvironment. Cancer Res. 2016;76(5):999-1008.
49. Grabner B, Schramek D, Mueller KM, et al. Disruption of STAT3 signalling promotes KRAS-induced lung tumorigenesis. Nat Commun. 2015;6:6285.
50. Dutta P, Sabri N, Li J, et al. Role of STAT3 in lung cancer. JAKSTAT. 2014;3(4): E999503.
51. Caetano MS, Zhang H, Cumpian AM, et al. IL6 blockade reprograms the lung tumor microenvironment to limit the development and progression of K-rasmutant lung cancer. Cancer Res. 2016;76(11):3189-3199.
52. Miklossy G, Hilliard TS, Turkson J. Therapeutic modulators of STAT signalling for human diseases. Nat Rev Drug Discov. 2013;12(8):611-629.
53. Yu H, Lee H, Herrmann A, et al. Revisiting STAT3 signalling in cancer: New and unexpected biological functions. Nat Rev Cancer. 2014;14(11):736-746.