Altered LKB1/CREB-regulated transcription co-activator (CRTC) signaling axis promotes esophageal cancer cell migration and invasion

Oncogene

Volumn 31, Issue 4, 2012, Pages 469-479

  Gu, Y ^a   Lin, S ^a   Li, J L ^b   Nakagawa, H ^c   Chen, Z ^a   Jin, B ^a   Tian, L ^a   Ucar, D A ^a   Shen, H ^a   Lu, J ^a   Hochwald, S N ^a   Kaye, F J ^a   Wu, L ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b BURNHAM INSTITUTE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CRTC co activator; Esophageal cancer; Invasion; LKB1; LYPD3; Migration

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; PROTEIN KINASE LKB1;

ARTICLE; CANCER CELL CULTURE; CARCINOGENICITY; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ESOPHAGUS CANCER; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR MECHANICS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL ADHESION MOLECULES; CELL LINE, TUMOR; CELL MOVEMENT; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ESOPHAGEAL NEOPLASMS; GPI-LINKED PROTEINS; HUMANS; NEOPLASM INVASIVENESS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84856215097     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.247     Document Type: Article

References (54)

1. Ahn S, Olive M, Aggarwal S, Krylov D, Ginty DD, Vinson C. (1998). A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Mol Cell Biol 18: 967-977. (Pubitemid 28063431)
2. Altarejos JY, Goebel N, Conkright MD, Inoue H, Xie J, Arias CM et al. (2008). The Creb1 coactivator Crtc1 is required for energy balance and fertility. Nat Med 14: 1112-1117.
3. JY, Montminy M. (2011). CREB and the CRTC coactivators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12: 141-151.
4. Andl CD, Mizushima T, Nakagawa H, Oyama K, Harada H, Chruma K et al. (2003). Epidermal growth factor receptor mediates increased cell proliferation, migration, and aggregation in esophageal keratinocytes in vitro and in vivo. J Biol Chem 278: 1824-1830. (Pubitemid 36801419)
5. Breuillaud L, Halfon O, Magistretti PJ, Pralong FP, Cardinaux J.R. (2009). Mouse fertility is not dependent on the CREB coactivator Crtc1. Nat Med 15: 989-990; author reply 991.
6. Carretero J, Medina PP, Pio R, Montuenga LM, Sanchez-Cespedes M. (2004). Novel and natural knockout lung cancer cell lines for the LKB1/STK11 tumor suppressor gene. Oncogene 23: 4037-4040. (Pubitemid 38747933)
7. Carretero J, Shimamura T, Rikova K, Jackson AL, Wilkerson MD, Borgman CL et al. (2010). Integrative genomic and proteomic analyses identify targets for Lkb1-deficient metastatic lung tumors. Cancer Cell 17: 547-559.
8. Chen J, Kesari S, Rooney C, Strack PR, Chen J, Shen H et al. (2010). Inhibition of Notch signaling blocks growht of glioblastoma cell lines and tumor. Genes Cancer 1: 822-835.
9. Chen Y, Li YH, Chen XP, Gong LM, Zhang SP, Chang ZJ et al. (2005). Point mutation at single tyrosine residue of novel oncogene NOK abrogates tumorigenesis in nude mice. Cancer Res 65: 10838-10846. (Pubitemid 41713351)
10. Conkright MD, Canettieri G, Screaton R, Guzman E, Miraglia L, Hogenesch JB et al. (2003). TORCs: transducers of regulated CREB activity. Mol Cell 12: 413-423. (Pubitemid 37238928)
11. Coxon A, Rozenblum E, Park YS, Joshi N, Tsurutani J, Dennis PA et al. (2005). Mect1-Maml2 fusion oncogene linked to the aberrant activation of cyclic AMP/CREB regulated genes. Cancer Res 65: 7137-7144. (Pubitemid 41161243)
12. Enzinger PC, Mayer RJ. (2003). Esophageal cancer. N Engl JMed 349: 2241-2252. (Pubitemid 37485141)
13. Esteller M, Avizienyte E, Corn PG, Lothe RA, Baylin SB, Aaltonen LA et al. (2000). Epigenetic inactivation of LKB1 in primary tumors associated with the Peutz-Jeghers syndrome. Oncogene 19: 164-168. (Pubitemid 30066364)
14. Giardiello FM, Brensinger JD, Tersmette AC, Goodman SN, Petersen GM, Booker SV et al. (2000). Very high risk of cancer in familial Peutz-Jeghers syndrome. Gastroenterology 119: 1447-1453. (Pubitemid 32198669)
15. Guldberg P, thor Straten P, Ahrenkiel V, Seremet T, Kirkin AF, Zeuthen J. (1999). Somatic mutation of the Peutz-Jeghers syndrome gene, LKB1/STK11, in malignant melanoM.A. Oncogene 18: 1777-1780. (Pubitemid 29137469)
16. Hansen LV, Laerum OD, Illemann M, Nielsen BS, Ploug M. (2008). Altered expression of the urokinase receptor homologue, C4.4A, in invasive areas of human esophageal squamous cell carcinoM.A. Int J Cancer 122: 734-741.
17. Hezel AF, Bardeesy N. (2008). LKB1; linking cell structure and tumor suppression. Oncogene 27: 6908-6919.
18. Iourgenko V, Zhang W, Mickanin C, Daly I, Jiang C, Hexham JM et al. (2003). Identification of a family of cAMP response elementbinding protein coactivators by genome-scale functional analysis in mammalian cells. Proc Natl Acad Sci USA 100: 12147-12152. (Pubitemid 37271529)
19. Ji H, Ramsey MR, Hayes DN, Fan C, McNamara K, Kozlowski P et al. (2007). LKB1 modulates lung cancer differentiation and metastasis. Nature 448: 807-810. (Pubitemid 47266337)
20. Jin J, Smith FD, Stark C, Wells CD, Fawcett JP, Kulkarni S et al. (2004). Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr Biol 14: 1436-1450. (Pubitemid 39123741)
21. Katoh Y, Takemori H, Lin XZ, TamuraM, MuraokaM, Satoh T et al. (2006). Silencing the constitutive active transcription factor CREB by the LKB1-SIK signaling cascade. FEBS J 273: 2730-2748.
22. Klein CA, Stoecklein NH. (2009). Lessons from an aggressive cancer: evolutionary dynamics in esophageal carcinoM.A. Cancer Res 69: 5285-5288.
23. Komiya T, Coxon A, Park Y, Chen WD, Zajac-Kaye M, Meltzer P et al. (2010). Enhanced activity of the CREB co-activator Crtc1 in LKB1 null lung cancer. Oncogene 29: 1672-1680.
24. Komiya T, Park Y, Modi S, Coxon AB, Oh H, Kaye FJ. (2006). Sustained expression of Mect1-Maml2 is essential for tumor cell growth in salivary gland cancers carrying the t(11;19) translocation. Oncogene 25: 6128-6132. (Pubitemid 44562411)
25. Kuwano H, Kato H, Miyazaki T, Fukuchi M, Masuda N, Nakajima M et al. (2005). Genetic alterations in esophageal cancer. Surg Today 35: 7-18. (Pubitemid 40941123)
26. Lam AK. (2000). Molecular biology of esophageal squamous cell carcinoM.A. Crit Rev Oncol Hematol 33: 71-90. (Pubitemid 30085471)
27. Launonen V, Avizienyte E, Loukola A, Laiho P, Salovaara R, Jarvinen H et al. (2000). No evidence of Peutz-Jeghers syndrome gene LKB1 involvement in left-sided colorectal carcinomas. Cancer Res 60: 546-548. (Pubitemid 30094548)
28. Lee JJ, Natsuizaka M, Ohashi S, Wong GS, Takaoka M, Michaylira CZ et al. (2010). Hypoxia activates the cyclooxygenase-2-prostaglandin E synthase axis. Carcinogenesis 31: 427-434.
29. Liu L, Yu XZ, Li TS, Song LX, Chen PL, Suo TL et al. (2004). A novel protein tyrosine kinase NOK that shares homology with platelet-derived growth factor/fibroblast growth factor receptors induces tumorigenesis and metastasis in nude mice. Cancer Res 64: 3491-3499. (Pubitemid 38657923)
30. Luo Z, Zang M, Guo W. (2010). AMPK as a metabolic tumor suppressor: control of metabolism and cell growth. Future Oncol 6: 457-470.
31. Mahoney CL, Choudhury B, Davies H, Edkins S, Greenman C, Haaften G et al. (2009). LKB1/KRAS mutant lung cancers constitute a genetic subset of NSCLC with increased sensitivity to MAPK and mTOR signalling inhibition. Br J Cancer 100: 370-375.
32. Makowski L, Hayes DN. (2008). Role of LKB1 in lung cancer development. Br J Cancer 99: 683-688.
33. Matsumoto S, Iwakawa R, Takahashi K, Kohno T, Nakanishi Y, Matsuno Y et al. (2007). Prevalence and specificity of LKB1 genetic alterations in lung cancers. Oncogene 26: 5911-5918.
34. Nishihira T, Hashimoto Y, Katayama M, Mori S, Kuroki T. (1993). Molecular and cellular features of esophageal cancer cells. J Cancer Res Clin Oncol 119: 441-449. (Pubitemid 23165049)
35. Paret C, Bourouba M, Beer A, Miyazaki K, Schnolzer M, Fiedler S et al. (2005). Ly6 family member C4.4A binds laminins 1 and 5, associates with galectin-3 and supports cell migration. Int J Cancer 115: 724-733. (Pubitemid 40776695)
36. Rodriguez LG, Wu X, Guan JL. (2005). Wound-healing assay. Methods Mol Biol 294: 23-29.
37. Rosel M, Claas C, Seiter S, Herlevsen M, Zoller M. (1998). Cloning and functional characterization of a new phosphatidyl-inositol anchored molecule of a metastasizing rat pancreatic tumor. Oncogene 17: 1989-2002. (Pubitemid 28488468)
38. Rowan A, Bataille V, MacKie R, Healy E, Bicknell D, Bodmer W et al. (1999). Somatic mutations in the Peutz-Jeghers (LKB1/STKII) gene in sporadic malignant melanomas. J Invest Dermatol 112: 509-511. (Pubitemid 29171943)
39. Rustgi AK. (2006). Models of esophageal carcinogenesis. Semin Oncol 33: S57-S58.
40. Sanchez-Cespedes M. (2007). A role for LKB1 gene in human cancer beyond the Peutz-Jeghers syndrome. Oncogene 26: 7825-7832. (Pubitemid 350261789)
41. Sanchez-Cespedes M, Parrella P, Esteller M, Nomoto S, Trink B, Engles JM et al. (2002). Inactivation of LKB1/STK11 is a common event in adenocarcinomas of the lung. Cancer Res 62: 3659-3662. (Pubitemid 34728843)
42. Sattler M, Mohi MG, Pride YB, Quinnan LR, Malouf NA, Podar K et al. (2002). Critical role for Gab2 in transformation by BCR/ABL. Cancer Cell 1: 479-492. (Pubitemid 41039128)
43. Seiter S, Stassar M, Rappl G, Reinhold U, Tilgen W, Zoller M. (2001). Upregulation of C4.4A expression during progression of melanoM.A. J Invest Dermatol 116: 344-347. (Pubitemid 32173741)
44. Shackelford DB, Shaw RJ. (2009). The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer 9: 563-575.
45. Shimada Y, Imamura M, Wagata T, Yamaguchi N, Tobe T. (1992). Characterization of 21 newly established esophageal cancer cell lines. Cancer 69: 277-284.
46. Tiainen M, Vaahtomeri K, Ylikorkala A, Makela TP. (2002). Growth arrest by the LKB1 tumor suppressor: induction of p21(WAF1/ CIP1). Hum Mol Genet 11: 1497-1504. (Pubitemid 34679250)
47. Tiainen M, Ylikorkala A, Makela TP. (1999). Growth suppression by Lkb1 is mediated by a G(1) cell cycle arrest. Proc Natl Acad Sci USA 96: 9248-9251. (Pubitemid 29374740)
48. Tonon G, Modi S, Wu L, Kubo A, Coxon AB, Komiya T et al. (2003). t(11;19)(q21;p13) translocation in mucoepidermoid carcinoma creates a novel fusion product that disrupts a Notch signaling pathway. Nat Genet 33: 208-213. (Pubitemid 36177076)
49. Vallbohmer D, Brabender J, Metzger R, Holscher AH. (2010). Genetics in the pathogenesis of esophageal cancer: possible predictive and prognostic factors. J Gastrointest Surg 14(Suppl 1): S75-S80.
50. van Lier MG, Wagner A, Mathus-Vliegen EM, Kuipers EJ, Steyerberg EW, van Leerdam ME. (2010). High cancer risk in Peutz-Jeghers syndrome: a systematic review and surveillance recommendations. Am J Gastroenterol 105: 1258-1264.
51. Wingo SN, Gallardo TD, Akbay EA, Liang MC, Contreras CM, Boren T et al. (2009). Somatic LKB1 mutations promote cervical cancer progression. PLoS One 4: e5137.
52. Wu L, Aster JC, Blacklow SC, Lake R, Artavanis-Tsakonas S, Griffin JD. (2000). MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nat Genet 26: 484-489.
53. Wu L, Liu J, Gao P, Nakamura M, Cao Y, Shen H et al. (2005). Transforming activity of MECT1-MAML2 fusion oncoprotein is mediated by constitutive CREB activation. EMBO J 24: 2391-2402. (Pubitemid 41032590)
54. Wurfel J, Seiter S, Stassar M, Claas A, Klas R, Rosel M et al. (2001). Cloning of the human homologue of the metastasis-associated rat C4.4A. Gene 262: 35-41. (Pubitemid 32155332)