Serine-arginine protein kinase 1 promotes a cancer stem cell-like phenotype through activation of Wnt/β-catenin signalling in NSCLC

Journal of Pathology

Volumn 240, Issue 2, 2016, Pages 184-196

  Gong, Liyun ^a   Song, Junwei ^a,b,c   Lin, Xi ^b   Wei, Fakai ^a   Zhang, Cuicui ^a   Wang, Zimei ^a   Zhu, Jinrong ^c   Wu, Shu ^b   Chen, Yu ^a   Liang, Jin ^a   Fu, XiaoYuan ^d   Lu, Junqiang ^d   Zhou, Chunhui ^e   Song, Libing ^b  

^a Shenzhen University School of Medicine   (China)

^b SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d SHENZHEN UNIVERSITY   (China)

^e GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

NSCLC; SRPK1; stem cell like phenotype; Wnt catenin signalling

Indexed keywords

BETA CATENIN; PHOSPHOTRANSFERASE; SERINE ARGININE PROTEIN KINASE 1; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL LINE; CANCER STEM CELL; CARCINOGENESIS; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE; GENE OVEREXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERINE ARGININE PROTEIN KINASE 1 GENE;

EID: 84988589109     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4767     Document Type: Article

References (49)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2007. CA Cancer J Clin 2007; 57: 43–66.
2. Travis LB, Curtis RE, Bennett WP, et al. Lung cancer after Hodgkin's disease. J Natl Cancer Inst 1995; 87: 1324-1327.
3. Wood SL, Pernemalm M, Crosbie PA, et al. The role of the tumor-microenvironment in lung cancer-metastasis and its relationship to potential therapeutic targets. Cancer Treatment Rev 2014; 40: 558–566.
4. Carnio S, Novello S, Papotti M, et al. Prognostic and predictive biomarkers in early stage non-small cell lung cancer: tumor based approaches including gene signatures. Transl Lung Cancer Res 2013; 2: 372–381.
5. Hoffman PC, Mauer AM, Vokes EE. Lung cancer. Lancet 2000; 355: 479–485.
6. al-Kattan K, Sepsas E, Fountain SW, et al. Disease recurrence after resection for stage I lung cancer. Eur J Cardiothorac Surg 1997; 12: 380–384.
7. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105–111.
8. Clarke MF. Oncogenes, self-renewal and cancer. Pathol Biol (Paris) 2006; 54: 109–111.
9. Pan CX, Zhu W, Cheng L. Implications of cancer stem cells in the treatment of cancer. Future Oncol 2006; 2: 723–731.
10. Yang W, Yan HX, Chen L, et al. Wnt/beta-catenin signaling contributes to activation of normal and tumorigenic liver progenitor cells. Cancer Res 2008; 68: 4287–4295.
11. Bartucci M, Svensson S, Romania P, et al. Therapeutic targeting of Chk1 in NSCLC stem cells during chemotherapy. Cell Death Differ 2011; 19: 768–778.
12. Seigel GM, Campbell LM, Narayan M, et al. Cancer stem cell characteristics in retinoblastoma. Mol Vis 2005; 11: 729–737.
13. Hemmati HD, Nakano I, Lazareff JA, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 2003; 100: 15178–15183.
14. Pelicci PG, Dalton P, Orecchia R. Heating cancer stem cells to reduce tumor relapse. Breast Cancer Res 2011; 13: 305.
15. Zhou B, Li Y, Deng Q, et al. SRPK1 contributes to malignancy of hepatocellular carcinoma through a possible mechanism involving PI3K/Akt. Mol Cell Biochem 2013; 379: 191–199.
16. Li XH, Song JW, Liu JL, et al. Serine-arginine protein kinase 1 is associated with breast cancer progression and poor patient survival. Med Oncol 2014; 31: 83.
17. Hayes GM, Carrigan PE, Beck AM, et al. Targeting the RNA splicing machinery as a novel treatment strategy for pancreatic carcinoma. Cancer Res 2006; 66: 3819–3827.
18. Chang Y, Wu Q, Tian T, et al. The influence of SRPK1 on glioma apoptosis, metastasis, and angiogenesis through the PI3K/Akt signaling pathway under normoxia. Tumour Biol 2015; 36:6083–6093.
19. Odunsi K, Mhawech-Fauceglia P, Andrews C, et al. Elevated expression of the serine-arginine protein kinase 1 gene in ovarian cancer and its role in cisplatin cytotoxicity in vitro. PLoS One 2012; 7: e51030.
20. Hayes GM, Carrigan PE, Miller LJ. Serine-arginine protein kinase 1 overexpression is associated with tumorigenic imbalance in mitogen-activated protein kinase pathways in breast, colonic, and pancreatic carcinomas. Cancer Res 2007; 67: 2072–2080.
21. Wu Q, Chang Y, Zhang L, et al. SRPK1 dissimilarly impacts on the growth, metastasis, chemosensitivity and angiogenesis of glioma in normoxic and hypoxic conditions. J Cancer 2013; 4: 727–735.
22. Gammons MV, Lucas R, Dean R, et al. Targeting SRPK1 to control VEGF-mediated tumour angiogenesis in metastatic melanoma. Br J Cancer 2014; 111: 477–485.
23. Lin JC, Lin CY, Tarn WY, et al. Elevated SRPK1 lessens apoptosis in breast cancer cells through RBM4-regulated splicing events. RNA 2014; 20: 1621–1631.
24. Corkery DP, Holly AC, Lahsaee S, et al. Connecting the speckles: splicing kinases and their role in tumorigenesis and treatment response. Nucleus 2015; 6: 279–288.
25. Amin EM, Oltean S, Hua J, et al. WT1 mutants reveal SRPK1 to be a downstream angiogenesis target by altering VEGF splicing. Cancer Cell 2011; 20: 768–780.
26. Sanidas I, Kotoula V, Ritou E, et al. The ratio of SRPK1/SRPK1a regulates erythroid differentiation in K562 leukaemic cells. Biochim Biophys Acta 2010; 1803: 1319–1331.
27. Zhou B, Li Y, Deng Q, et al. SRPK1 contributes to malignancy of hepatocellular carcinoma through a possible mechanism involving PI3K/Akt. Mol Cell Biochem 2013; 379: 191–199.
28. Ibrahim L, Dominguez M, Yacoub M. Primary human adult lung epithelial cells in vitro: response to interferon-gamma and cytomegalovirus. Immunology 1993; 79: 119–124.
29. Greene FL. AJCC Cancer Staging Handbook. From the AJCC Cancer Staging Manual (6th edn), Greene FL, Page DL, Fleming ID, et al (eds). Springer Science+Business Media New York, 2002.
30. Li J, Zhang N, Song L-B, et al. Astrocyte elevated gene-1 is a novel prognostic marker for breast cancer progression and overall patient survival. Clin Cancer Res 2008; 14: 3319–3326.
31. Li J, Gong L-Y, Song L-B, et al. Oncoprotein Bmi-1 renders apoptotic resistance to glioma cells through activation of the IKK-nuclear factor-kB pathway. Am J Pathol 2010; 176: 699–709.
32. Hahn WC, Dessain SK, Brooks MW, et al. Enumeration of the simian virus 40 early region elements necessary for human cell transformation. Mol Cell Biol 2002; 22: 2111–2123.
33. Beckett WS. Epidemiology and etiology of lung cancer. Clin Chest Med 1993; 14: 1–15.
34. Maugeri-Saccà M, Vici P, Di Lauro L, et al. Cancer stem cells: are they responsible for treatment failure? Future Oncol 2014; 10: 2033–2044.
35. Takubo K, Ohmura M, Azuma M, et al. Stem cell defects in ATM-deficient undifferentiated spermatogonia through DNA damage-induced cell-cycle arrest. Cell Stem Cell 2008; 2: 170–182.
36. Gui JF, Lane WS, Fu XD. A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 1994; 369: 678–682.
37. Giannakouros T, Nikolakaki E, Mylonis I, et al. Serine-arginine protein kinases: a small protein kinase family with a large cellular presence. FEBS J 2011; 278: 570–586.
38. Long JC, Caceres JF. The SR protein family of splicing factors: master regulators of gene expression. Biochem J 2009; 417: 15–27.
39. Brinkman BM. Splice variants as cancer biomarkers. Clin Biochem 2004; 37: 584–594.
40. Venables JP. Aberrant and alternative splicing in cancer. Cancer Res 2004; 64: 7647–7654.
41. Srebrow A, Kornblihtt AR. The connection between splicing and cancer. J Cell Sci 2006; 119: 2635–2641.
42. Xi L, Feber A, Gupta V, et al. Whole genome exon arrays identify differential expression of alternatively spliced, cancer-related genes in lung cancer. Nucleic Acids Res 2008; 36: 6535–6547.
43. Mavrou A, Brakspear K, Hamdollah-Zadeh M, et al. Serine-arginine protein kinase 1 (SRPK1) inhibition as a potential novel targeted therapeutic strategy in prostate cancer. Oncogene 2015; 34: 4311–4319.
44. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010; 29: 4741–4751.
45. Li S, Li Q. Cancer stem cells and tumor metastasis (Review). Int J Oncol 2014; 44: 1806–1812.
46. DiMeo TA, Anderson K, Phadke P, et al. A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial–mesenchymal transition in basal-like breast cancer. Cancer Res 2009; 69: 5364–5373.
47. Liu C, Li Y, Semenov M, et al. Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002; 108: 837–847.
48. Fu Y, Zheng S, An N, et al. Beta-catenin as a potential key target for tumor suppression. Int J Cancer 2011; 129: 1541–1551.
49. Gangaraju VK, Lin H. MicroRNAs: key regulators of stem cells. Nature Rev Mol Cell Biol 2009; 10: 116–125.