Low spinophilin expression enhances aggressive biological behavior of breast cancer

Oncotarget

Volumn 6, Issue 13, 2015, Pages 11191-11202

  Schwarzenbacher, Daniela ^a   Stiegelbauer, Verena ^a   Deutsch, Alexander ^a   Ress, Anna Lena ^a   Aigelsreiter, Ariane ^a   Schauer, Silvia ^a   Wagner, Karin ^a   Langsenlehner, Tanja ^a   Resel, Margit ^a   Gerger, Armin ^a   Ling, Hui ^b   Ivan, Cristina ^b   Calin, George Adrian ^b   Hoefler, Gerald ^a   Rinner, Beate ^a   Pichler, Martin ^a,b  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Breast cancer; Cellular growth; Invasion; Prognosis; Tumor suppressor

Indexed keywords

SPINOPHILIN; ACTIN BINDING PROTEIN; MESSENGER RNA; NERVE PROTEIN; NEURABIN; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER SURVIVAL; CELL GROWTH; CELL MIGRATION; CELL RENEWAL; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GROWTH RATE; IN VIVO STUDY; LUNG METASTASIS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR INVASION; UPREGULATION; ANIMAL; BREAST TUMOR; CANCER STAGING; CELL MOTION; CELL PROLIFERATION; CELL TRANSFORMATION; DRUG SCREENING; ENZYME IMMUNOASSAY; GENE EXPRESSION PROFILING; GENETICS; HUMAN; METABOLISM; MORTALITY; NONOBESE DIABETIC MOUSE; PATHOLOGY; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; SURVIVAL RATE; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BIOMARKERS, TUMOR; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; MICE; MICE, INBRED NOD; MICE, SCID; MICROFILAMENT PROTEINS; NEOPLASM STAGING; NERVE TISSUE PROTEINS; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SURVIVAL RATE; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84929649415     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3586     Document Type: Article

References (44)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61(2):69-90.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63(1):11-30.
3. Lorico A, Rappa G. Phenotypic heterogeneity of breast cancer stem cells. J Oncol 2011;2011:135039.
4. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature 2000;406(6797):747-52.
5. 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(19):10869-74.
6. Prat A, Adamo B, Cheang MC, Anders CK, Carey LA, Perou CM. Molecular characterization of basal-like and non-basal-like triple-negative breast cancer. Oncologist 2013;18(2):123-33.
7. Carnero A. Spinophilin: A new tumor suppressor at 17q21. Curr Mol Med 2012;12(5):528-35.
8. Ferrer I, Peregrino S, Canamero M, Cecilia Y, Blanco-Aparicio C, Carnero A. Spinophilin loss contributes to tumorigenesis in vivo. Cell Cycle 2011;10(12):1948-55.
9. Molina-Pinelo S, Ferrer I, Blanco-Aparicio C, Peregrino S, Pastor MD, Alvarez-Vega J, et al. Down-regulation of spinophilin in lung tumours contributes to tumourigenesis. J Pathol 2011;225(1):73-82.
10. Aigelsreiter A, Ress AL, Bettermann K, Schauer S, Koller K, Eisner F, et al. Low expression of the putative tumour suppressor spinophilin is associated with higher proliferative activity and poor prognosis in patients with hepatocellular carcinoma. Br J Cancer 2013;108(9):1830-7.
11. Aigelsreiter AM, Aigelsreiter A, Wehrschuetz M, Ress AL, Koller K, Salzwimmer M, et al. Loss of the putative tumor suppressor protein spinophilin is associated with poor prognosis in head and neck cancer. Hum Pathol 2014;45(4):683-90.
12. Estevez-Garcia P, Lopez-Calderero I, Molina-Pinelo S, Munoz-Galvan S, Salinas A, Gomez-Izquierdo L, et al. Spinophilin loss correlates with poor patient prognosis in advanced stages of colon carcinoma. Clin Cancer Res 2013;19(14):3925-35.
13. Kao J, Salari K, Bocanegra M, Choi YL, Girard L, Gandhi J, et al. Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 2009;4(7):e6146.
14. Wasielewski M, Elstrodt F, Klijn JG, Berns EM, Schutte M. Thirteen new p53 gene mutants identified among 41 human breast cancer cell lines. Breast Cancer Res Treat 2006;99(1):97-101.
15. Allen PB, Ouimet CC, Greengard P. Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci U S A 1997;94(18):9956-61.
16. Satoh A, Nakanishi H, Obaishi H, Wada M, Takahashi K, Satoh K, et al. Neurabin-II/spinophilin. an actin filament-binding protein with one pdz domain localized at cadherin-based cell-cell adhesion sites. J Biol Chem 1998;273(6):3470-5.
17. Sakisaka T, Nakanishi H, Takahashi K, Mandai K, Miyahara M, Satoh A, et al. Different behavior of l-afadin and neurabin-II during the formation and destruction of cell-cell adherens junction. Oncogene 1999;18(8):1609-17.
18. Vivo M, Calogero RA, Sansone F, Calabro V, Parisi T, Borrelli L, et al. The human tumor suppressor arf interacts with spinophilin/neurabin II, a type 1 protein-phosphatasebinding protein. J Biol Chem 2001;276(17):14161-9.
19. Santra M, Zhang X, Santra S, Jiang F, Chopp M. Ectopic doublecortin gene expression suppresses the malignant phenotype in glioblastoma cells. Cancer Res 2006;66(24):11726-35.
20. Santra M, Santra S, Buller B, Santra K, Nallani A, Chopp M. Effect of doublecortin on self-renewal and differentiation in brain tumor stem cells. Cancer Sci 2011;102(7):1350-7.
21. Ress AL, Stiegelbauer V, Schwarzenbacher D, Deutsch A, Perakis S, Ling H, et al. Spinophilin expression determines cellular growth, cancer stemness and 5-flourouracil resistance in colorectal cancer. Oncotarget 2014;5(18):8492-502.
22. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/ progenitor cells. Genes Dev 2003;17(10):1253-70.
23. Grimshaw MJ, Cooper L, Papazisis K, Coleman JA, Bohnenkamp HR, Chiapero-Stanke L, et al. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res 2008;10(3):R52.
24. Chen YT, Alpen B, Ono T, Gure AO, Scanlan MA, Biggs WH,3rd, et al. Identification and characterization of mouse SSX genes: A multigene family on the X chromosome with restricted cancer/testis expression. Genomics 2003;82(6):628-36.
25. Dubovsky JA, McNeel DG. Inducible expression of a prostate cancer-testis antigen, SSX-2, following treatment with a DNA methylation inhibitor. Prostate 2007;67(16):1781-90.
26. Naka N, Joyama S, Tsukamoto Y, Yoshioka K, Hashimoto N, Ujiiye T, et al. Quantification of SSX mRNA expression in human bone and soft tissue tumors using nucleic acid sequence-based amplification. J Mol Diagn 2005;7(2):187-97.
27. Chen L, Zhou WB, Zhao Y, Liu XA, Ding Q, Zha XM, et al. Cancer/testis antigen SSX2 enhances invasiveness in MCF-7 cells by repressing ERalpha signaling. Int J Oncol 2012;40(6):1986-94.
28. Cernaro V, Lacquaniti A, Lupica R, Buemi A, Trimboli D, Giorgianni G, et al. Relaxin: New pathophysiological aspects and pharmacological perspectives for an old protein. Med Res Rev 2014;34(1):77-105.
29. Hombach-Klonisch S, Bialek J, Radestock Y, Truong A, Agoulnik AI, Fiebig B, et al. INSL3 has tumor-promoting activity in thyroid cancer. Int J Cancer 2010;127(3):521-31.
30. Klonisch T, Bialek J, Radestock Y, Hoang-Vu C, Hombach-Klonisch S. Relaxin-like ligand-receptor systems are autocrine/paracrine effectors in tumor cells and modulate cancer progression and tissue invasiveness. Adv Exp Med Biol 2007;612:104-18.
31. Chiang DY, Li N, Wang Q, Alsina K, Quick A, Reynolds JO, et al. Impaired local regulation of ryanodine receptor type-2 by protein phosphatase 1 promotes atrial fibrillation. Cardiovasc Res 2014; 103(1):178-87.
32. Kobylewski SE, Henderson KA, Eckhert CD. Identification of ryanodine receptor isoforms in prostate DU-145, LNCaP, and PWR-1E cells. Biochem Biophys Res Commun 2012;425(2):431-5.
33. Davis FM, Parsonage MT, Cabot PJ, Parat MO, Thompson EW, Roberts-Thomson SJ, et al. Assessment of gene expression of intracellular calcium channels, pumps and exchangers with epidermal growth factor-induced epithelial-mesenchymal transition in a breast cancer cell line. Cancer Cell Int 2013;13(1):76,2867-13-76.
34. Abdul M, Ramlal S, Hoosein N. Ryanodine receptor expression correlates with tumor grade in breast cancer. Pathol Oncol Res 2008;14(2):157-60.
35. Parker BS, Ciocca DR, Bidwell BN, Gago FE, Fanelli MA, George J, et al. Primary tumour expression of the cysteine cathepsin inhibitor stefin A inhibits distant metastasis in breast cancer. J Pathol 2008;214(3):337-46.
36. Lee S, Stewart S, Nagtegaal I, Luo J, Wu Y, Colditz G, et al. Differentially expressed genes regulating the progression of ductal carcinoma in situ to invasive breast cancer. Cancer Res 2012;72(17):4574-86.
37. Berditchevski F. Complexes of tetraspanins with integrins:More than meets the eye. J Cell Sci 2001;114(Pt 23):4143-51.
38. Latil A, Chene L, Cochant-Priollet B, Mangin P, Fournier G, Berthon P, et al. Quantification of expression of netrins, slits and their receptors in human prostate tumors. Int J Cancer 2003;103(3):306-15.
39. Buckley NE, D'Costa Z, Kaminska M, Mullan PB. S100A2 is a BRCA1/p63 coregulated tumour suppressor gene with roles in the regulation of mutant p53 stability. Cell Death Dis 2014;5:e1070.
40. Teoh SS, Whisstock JC, Bird PI. Maspin (SERPINB5) is an obligate intracellular serpin. J Biol Chem 2010;285(14):10862-9.
41. Vecchi M, Confalonieri S, Nuciforo P, Vigano MA, Capra M, Bianchi M, et al. Breast cancer metastases are molecularly distinct from their primary tumors. Oncogene 2008;27(15):2148-58.
42. Pellatt AJ, Wolff RK, John EM, Torres-Mejia G, Hines LM, Baumgartner KB, et al. SEPP1 influences breast cancer risk among women with greater native american ancestry: The breast cancer health disparities study. PLoS One 2013;8(11):e80554.
43. Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature 2012;490(7418):61-70.
44. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001;25(4):402-8.