p90 ribosomal S6 kinase 2 promotes invasion and metastasis of human head and neck squamous cell carcinoma cells

Journal of Clinical Investigation

Volumn 120, Issue 4, 2010, Pages 1165-1177

  Kang, Sumin ^a   Elf, Shannon ^a   Lythgoe, Katherine ^a   Hitosugi, Taro ^a   Taunton, Jack ^b   Zhou, Wei ^a   Xiong, Li ^a   Wang, Dongsheng ^a   Muller, Susan ^c   Fan, Songqing ^a   Sun, Shi Yong ^a   Marcus, Adam I ^a   Gu, Ting Lei ^d   Polakiewicz, Roberto D ^d   Chen, Zhuo ^a   Khuri, Fadlo R ^a   Shin, Dong M ^a   Chen, Jing ^a  

^a EMORY UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CELL SIGNALING TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HEAT SHOCK PROTEIN 27; PROTEIN P90; S6 KINASE; S6 KINASE 2; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INVASION; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DOWN REGULATION; ENZYME ACTIVATION; HEAD AND NECK CARCINOMA; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SQUAMOUS CELL CARCINOMA; XENOGRAFT;

ACTINS; ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DISEASE PROGRESSION; HEAD AND NECK NEOPLASMS; HSP27 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHATIC METASTASIS; MICE; NEOPLASM INVASIVENESS; PHOSPHORYLATION; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; RNA, SMALL INTERFERING;

EID: 77951189135     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI40582     Document Type: Article

References (51)

1. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell. 2006;127(4):679-695.
2. Nguyen DX, Massague J. Genetic determinants of cancer metastasis. Nat Rev Genet. 2007;8(5):341-352.
3. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer. 2003;3(6):453-458.
4. Haddad RI, Shin DM. Recent advances in head and neck cancer. N Engl J Med. 2008;359(11):1143-1154.
5. Ursini-Siegel J, Schade B, Cardiff RD, Muller WJ. Insights from transgenic mouse models of ERBB2-induced breast cancer. Nat Rev Cancer. 2007;7(5):389-397.
6. Blenis J. Signal transduction via the MAP kinases: proceed at your own RSK. Proc Natl Acad Sci U S A. 1993;90(13):5889-5892.
7. Frodin M, Gammeltoft S. Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol Cell Endocrinol. 1999;151(1-2):65-77.
8. Buck M, Poli V, Hunter T, Chojkier M. C/EBPbeta phosphorylation by RSK creates a functional XEXD caspase inhibitory box critical for cell survival. Mol Cell. 2001;8(4):807-816.
9. He Z, Ma WY, Liu G, Zhang Y, Bode AM, Dong Z. Arsenite-induced phosphorylation of histone H3 at serine 10 is mediated by Akt1, extracellular signal-regulated kinase 2, and p90 ribosomal S6 kinase 2 but not mitogen- and stress-activated protein kinase 1. J Biol Chem. 2003;278(12):10588-10593.
10. Palmer A, Gavin AC, Nebreda AR. A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase Myt1. EMBO J. 1998;17(17):5037-5047.
11. Shimamura A, Ballif BA, Richards SA, Blenis J. Rsk1 mediates a MEK-MAP kinase cell survival signal. Curr Biol. 2000;10(3):127-135.
12. Dehan E, et al. betaTrCP- and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Mol Cell. 2009; 33(1):109-116.
13. Anjum R, Roux PP, Ballif BA, Gygi SP, Blenis J. The tumor suppressor DAP kinase is a target of RSK-mediated survival signaling. Curr Biol. 2005; 15(19):1762-1767.
14. Cohen MS, Zhang C, Shokat KM, Taunton J. Structural bioinformatics-based design of selective, irreversible kinase inhibitors. Science. 2005; 308(5726):1318-1321.
15. Cohen MS, Hadjivassiliou H, Taunton J. A clickable inhibitor reveals context-dependent autoactivation of p90 RSK. Nat Chem Biol. 2007;3(3):156-160.
16. Sapkota GP, et al. BI-D1870 is a specific inhibitor of the p90 RSK (ribosomal S6 kinase) isoforms in vitro and in vivo. Biochem J. 2007;401(1):29-38.
17. Zhang X, et al. A lymph node metastatic mouse model reveals alterations of metastasis-related gene expression in metastatic human oral carcinoma sublines selected from a poorly metastatic parental cell line. Cancer. 2002;95(8):1663-1672.
18. Xing J, Ginty DD, Greenberg ME. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science. 1996;273(5277):959-963.
19. Jean D, Bar-Eli M. Regulation of tumor growth and metastasis of human melanoma by the CREB transcription factor family. Mol Cell Biochem. 2000; 212(1-2):19-28.
20. Jean D, et al. Inhibition of tumor growth and metastasis of human melanoma by intracellular anti- ATF-1 single chain Fv fragment. Oncogene. 2000; 19(22):2721-2730.
21. Jean D, Harbison M, McConkey DJ, Ronai Z, Bar- Eli M. CREB and its associated proteins act as survival factors for human melanoma cells. J Biol Chem. 1998;273(38):24884-24890.
22. Xie S, Price JE, Luca M, Jean D, Ronai Z, Bar-Eli M. Dominant-negative CREB inhibits tumor growth and metastasis of human melanoma cells. Oncogene. 1997;15(17):2069-2075. (Pubitemid 27489134)
23. Miron T, Vancompernolle K, Vandekerckhove J, Wilchek M, Geiger B. A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein. J Cell Biol. 1991;114(2):255-261.
24. Zhang D, Wong LL, Koay ES. Phosphorylation of Ser78 of Hsp27 correlated with HER-2/neu status and lymph node positivity in breast cancer. Mol Cancer. 2007;6:52.
25. Shin KD, et al. Blocking tumor cell migration and invasion with biphenyl isoxazole derivative KRIBB3, a synthetic molecule that inhibits Hsp27 phosphorylation. J Biol Chem. 2005;280(50):41439-41448.
26. Gerthoffer WT, Gunst SJ. Invited review: focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol. 2001;91(2):963-972.
27. Landry J, Huot J. Modulation of actin dynamics during stress and physiological stimulation by a signaling pathway involving p38 MAP kinase and heat-shock protein 27. Biochem Cell Biol. 1995; 73(9-10):703-707.
28. Gabarra-Niecko V, Schaller MD, Dunty JM. FAK regulates biological processes important for the pathogenesis of cancer. Cancer Metastasis Rev. 2003; 22(4):359-374.
29. Mon NN, Ito S, Senga T, Hamaguchi M. FAK signaling in neoplastic disorders: a linkage between inflammation and cancer. Ann N Y Acad Sci. 2006; 1086:199-212.
30. Maina F, et al. Uncoupling of Grb2 from the Met receptor in vivo reveals complex roles in muscle development. Cell. 1996;87(3):531-542.
31. Bardelli A, et al. Uncoupling signal transducers from oncogenic MET mutants abrogates cell transformation and inhibits invasive growth. Proc Natl Acad Sci U S A. 1998;95(24):14379-14383.
32. Takayama H, et al. Diverse tumorigenesis associated with aberrant development in mice overexpressing hepatocyte growth factor/scatter factor. Proc Natl Acad Sci U S A. 1997;94(2):701-706.
33. Rong S, Segal S, Anver M, Resau JH, Vande Woude GF. Invasiveness and metastasis of NIH 3T3 cells induced by Met-hepatocyte growth factor/scatter factor autocrine stimulation. Proc Natl Acad Sci U S A. 1994;91(11):4731-4735.
34. Wu D, et al. cAMP-responsive element-binding protein regulates vascular endothelial growth factor expression: implication in human prostate cancer bone metastasis. Oncogene. 2007;26(35):5070-5077.
35. Benjamin IJ, McMillan DR. Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res. 1998;83(2):117-132.
36. Arrigo AP, et al. Hsp27 (HspB1) and alphaB-crystallin (HspB5) as therapeutic targets. FEBS Lett. 2007;581(19):3665-3674.
37. Garrido C, Brunet M, Didelot C, Zermati Y, Schmitt E, Kroemer G. Heat shock proteins 27 and 70: antiapoptotic proteins with tumorigenic properties. Cell Cycle. 2006;5(22):2592-2601.
38. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J. Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylationinduced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol. 1995;15(1):505-516.
39. Geum D, Son GH, Kim K. Phosphorylation-dependent cellular localization and thermoprotective role of heat shock protein 25 in hippocampal progenitor cells. J Biol Chem. 2002;277(22):19913-19921.
40. Kang S, et al. FGFR3 activates RSK2 to mediate hematopoietic transformation through tyrosine phosphorylation of RSK2 and activation of the MEK/ ERK pathway. Cancer Cell. 2007;12(3):201-214.
41. Gibson SL, Ma Z, Shaw LM. Divergent roles for IRS-1 and IRS-2 in breast cancer metastasis. Cell Cycle. 2007;6(6):631-637.
42. Ma Z, Gibson SL, Byrne MA, Zhang J, White MF, Shaw LM. Suppression of insulin receptor substrate 1 (IRS-1) promotes mammary tumor metastasis. Mol Cell Biol. 2006;26(24):9338-9351.
43. Zhang Y, et al. c-Jun, a crucial molecule in metastasis of breast cancer and potential target for biotherapy. Oncol Rep. 2007;18(5):1207-1212.
44. Zhang Y, et al. Critical role of c-Jun overexpression in liver metastasis of human breast cancer xenograft model. BMC Cancer. 2007;7:145.
45. Robinson CM, et al. Overexpression of JunB in undifferentiated malignant rat oral keratinocytes enhances the malignant phenotype in vitro without altering cellular differentiation. Int J Cancer. 2001; 91(5):625-630.
46. Benvenuti S, Comoglio PM. The MET receptor tyrosine kinase in invasion and metastasis. J Cell Physiol. 2007;213(2):316-325.
47. Furge KA, Zhang YW, Vande Woude GF. Met receptor tyrosine kinase: enhanced signaling through adapter proteins. Oncogene. 2000;19(49):5582-5589.
48. Ma PC, Maulik G, Christensen J, Salgia R. c-Met: structure, functions and potential for therapeutic inhibition. Cancer Metastasis Rev. 2003;22(4):309-325.
49. Baldassarre G, et al. p27(Kip1)-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell. 2005;7(1):51-63.
50. Platet N, Cathiard AM, Gleizes M, Garcia M. Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. Crit Rev Oncol Hematol. 2004;51(1):55-67.
51. Chen AG, Yu ZC, Yu XF, Cao WF, Ding F, Liu ZH. Overexpression of Ets-like protein 1 in human esophageal squamous cell carcinoma. World J Gastroenterol. 2006;12(48):7859-7863. (Pubitemid 46099960)