932
Views
4
CrossRef citations to date
0
Altmetric
Report

Epithelial morphological reversion drives Profilin-1-induced elevation of p27kip1 in mesenchymal triple-negative human breast cancer cells through AMP-activated protein kinase activation

, , , &
Pages 2914-2923 | Received 29 Apr 2015, Accepted 01 Jul 2015, Published online: 22 Aug 2015

References

  • Yamaguchi H, Condeelis J. Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta 2007; 1773:642-52; PMID:16926057; http://dx.doi.org/10.1016/j.bbamcr.2006.07.001
  • Mouneimne G, Hansen SD, Selfors LM, Petrak L, Hickey MM, Gallegos LL, Simpson KJ, Lim J, Gertler FB, Hartwig JH, et al. Differential remodeling of actin cytoskeleton architecture by profilin isoforms leads to distinct effects on cell migration and invasion. Cancer Cell 2012; 22:615-30; PMID:23153535; http://dx.doi.org/10.1016/j.ccr.2012.09.027
  • Stevenson RP, Veltman D, Machesky LM. Actin-bundling proteins in cancer progression at a glance. J Cell Sci 2012; 125:1073-9; PMID:22492983; http://dx.doi.org/10.1242/jcs.093799
  • Gross SR. Actin binding proteins: their ups and downs in metastatic life. Cell Adh Migr 2013; 7:199-213; PMID:23302954; http://dx.doi.org/10.4161/cam.23176
  • Janke J, Schluter K, Jandrig B, Theile M, Kölble K, Arnold W, Grinstein E, Schwartz A, Estevéz-Schwarz L, Schlag PM, et al. Suppression of tumorigenicity in breast cancer cells by the microfilament protein profilin 1. J Exp Med 2000; 191:1675-86; PMID:10811861; http://dx.doi.org/10.1084/jem.191.10.1675
  • Ding Z, Joy M, Bhargava R, Gunsaulus M, Lakshman N, Miron-Mendoza M, Petroll M, Condeelis J, Wells A, Roy P. Profilin-1 downregulation has contrasting effects on early vs late steps of breast cancer metastasis. Oncogene 2014; 33:2065-74; PMID:23686314; http://dx.doi.org/10.1038/onc.2013.166
  • Valenzuela-Iglesias A, Sharma VP, Beaty BT, Ding Z, Gutierrez-Millan LE, Roy P, Condeelis JS, Bravo-Cordero JJ. Profilin1 regulates invadopodium maturation in human breast cancer cells. Eur J Cell Biol 2015; 94:78-89; PMID:25613364; http://dx.doi.org/10.1016/j.ejcb.2014.12.002
  • Zou L, Jaramillo M, Whaley D, Wells A, Panchapakesa V, Das T, Roy P. Profilin-1 is a negative regulator of mammary carcinoma aggressiveness. Br J Cancer 2007; 97:1361-71; PMID:17940506; http://dx.doi.org/10.1038/sj.bjc.6604038
  • Coumans JV, Gau D, Poljak A, Wasinger V, Roy P, Moens PD. Profilin-1 overexpression in MDA-MB-231 breast cancer cells is associated with alterations in proteomics biomarkers of cell proliferation, survival, and motility as revealed by global proteomics analyses. OMICS 2014; 18:778-91; PMID:25454514; http://dx.doi.org/10.1089/omi.2014.0075
  • Chu IM, Hengst L, Slingerland JM. The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy. Nat Rev Cancer 2008; 8:253-67; PMID:18354415; http://dx.doi.org/10.1038/nrc2347
  • Zou L, Ding Z, Roy P. Profilin-1 overexpression inhibits proliferation of MDA-MB-231 breast cancer cells partly through p27kip1 upregulation. J Cell Physiol 2010; 223:623-9; PMID:20143334
  • Vervoorts J, Luscher B. Post-translational regulation of the tumor suppressor p27(KIP1). Cell Mol Life Sci 2008; 65:3255-64; PMID:18636226; http://dx.doi.org/10.1007/s00018-008-8296-7
  • Nacusi LP, Sheaff RJ. Akt1 sequentially phosphorylates p27kip1 within a conserved but non-canonical region. Cell Div 2006; 1:11; PMID:16780593; http://dx.doi.org/10.1186/1747-1028-1-11
  • Larrea MD, Liang J, Da Silva T, Hong F, Shao SH, Han K, Dumont D, Slingerland JM. Phosphorylation of p27Kip1 regulates assembly and activation of cyclin D1-Cdk4. Mol Cell Biol 2008; 28:6462-72; PMID:18710949; http://dx.doi.org/10.1128/MCB.02300-07
  • Gao D, Inuzuka H, Tseng A, Chin RY, Toker A, Wei W. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat Cell Biol 2009; 11:397-408; PMID:19270695; http://dx.doi.org/10.1038/ncb1847
  • Liang J, Shao SH, Xu ZX, Hennessy B, Ding Z, Larrea M, Kondo S, Dumont DJ, Gutterman JU, Walker CL, et al. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 2007; 9:218-24; PMID:17237771; http://dx.doi.org/10.1038/ncb1537
  • Tsvetkov LM, Yeh KH, Lee SJ, Sun H, Zhang H. p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. Curr Biol 1999; 9:661-4; PMID:10375532; http://dx.doi.org/10.1016/S0960-9822(99)80290-5
  • Hershko DD. Oncogenic properties and prognostic implications of the ubiquitin ligase Skp2 in cancer. Cancer 2008; 112:1415-24; PMID:18260093; http://dx.doi.org/10.1002/cncr.23317
  • Schiappacassi M, Lovisa S, Lovat F, Fabris L, Colombatti A, Belletti B, Baldassarre G. Role of T198 modification in the regulation of p27(Kip1) protein stability and function. PloS One 2011; 6:e17673; PMID:21423803; http://dx.doi.org/10.1371/journal.pone.0017673
  • Shanmugasundaram K, Block K, Nayak BK, Livi CB, Venkatachalam MA, Sudarshan S. PI3K regulation of the SKP-2/p27 axis through mTORC2. Oncogene 2013; 32:2027-36; PMID:22733130; http://dx.doi.org/10.1038/onc.2012.226
  • Maddika S, Ande SR, Wiechec E, Hansen LL, Wesselborg S, Los M. Akt-mediated phosphorylation of CDK2 regulates its dual role in cell cycle progression and apoptosis. J Cell Sci 2008; 121:979-88; PMID:18354084; http://dx.doi.org/10.1242/jcs.009530
  • Bae YH, Ding Z, Das T, Wells A, Gertler F, Roy P. Profilin1 regulates PI(3,4)P2 and lamellipodin accumulation at the leading edge thus influencing motility of MDA-MB-231 cells. Proc Natl Acad Sci U S A 2010; 107:21547-52; PMID:21115820; http://dx.doi.org/10.1073/pnas.1002309107
  • Das T, Bae YH, Wells A, Roy P. Profilin-1 overexpression upregulates PTEN and suppresses AKT activation in breast cancer cells. J Cell Physiol 2009; 218:436-43; PMID:18937284; http://dx.doi.org/10.1002/jcp.21618
  • Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P. The selectivity of protein kinase inhibitors: a further update. Biochem J 2007; 408:297-315; PMID:17850214; http://dx.doi.org/10.1042/BJ20070797
  • Zou L, Hazan R, Roy P. Profilin-1 overexpression restores adherens junctions in MDA-MB-231 breast cancer cells in R-cadherin-dependent manner. Cell Motil Cytoskeleton 2009; 66:1048-56; PMID:19593789; http://dx.doi.org/10.1002/cm.20407
  • Wittenmayer N, Jandrig B, Rothkegel M, Schlüter K, Arnold W, Haensch W, Scherneck S, Jockusch BM. Tumor suppressor activity of profilin requires a functional actin binding site. Mol Biol Cell 2004; 15:1600-8; PMID:14767055; http://dx.doi.org/10.1091/mbc.E03-12-0873
  • Berx G, Cleton-Jansen AM, Nollet F, de Leeuw WJ, van de Vijver M, Cornelisse C, van Roy F. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J 1995; 14:6107-15; PMID:8557030
  • Hennig G, Behrens J, Truss M, Frisch S, Reichmann E, Birchmeier W. Progression of carcinoma cells is associated with alterations in chromatin structure and factor binding at the E-cadherin promoter in vivo. Oncogene 1995; 11:475-84; PMID:7630631
  • Hirohashi S. Inactivation of the E-cadherin-mediated cell adhesion system in human cancers. Am J Pathol 1998; 153:333-9; PMID:9708792; http://dx.doi.org/10.1016/S0002-9440(10)65575-7
  • Yokoyama K, Kamata N, Hayashi E, Hoteiya T, Ueda N, Fujimoto R, Nagayama M. Reverse correlation of E-cadherin and snail expression in oral squamous cell carcinoma cells in vitro. Oral Oncol 2001; 37:65-71; PMID:11120485; http://dx.doi.org/10.1016/S1368-8375(00)00059-2
  • Yoshiura K, Kanai Y, Ochiai A, Shimoyama Y, Sugimura T, Hirohashi S. Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas. Proc Natl Acad Sci U S A 1995; 92:7416-9; PMID:7543680; http://dx.doi.org/10.1073/pnas.92.16.7416
  • Birchmeier W, Behrens J. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim Biophys Acta 1994; 1198:11-26; PMID:8199193
  • St Croix B, Sheehan C, Rak JW, Florenes VA, Slingerland JM, Kerbel RS. E-Cadherin-dependent growth suppression is mediated by the cyclin-dependent kinase inhibitor p27(KIP1). J Cell Biol 1998; 142:557-71; PMID:9679152; http://dx.doi.org/10.1083/jcb.142.2.557
  • Agiostratidou G, Li M, Suyama K, Badano I, Keren R, Chung S, Anzovino A, Hulit J, Qian B, Bouzahzah B, et al. Loss of retinal cadherin facilitates mammary tumor progression and metastasis. Cancer Res 2009; 69:5030-8; PMID:19491271; http://dx.doi.org/10.1158/0008-5472.CAN-08-4007
  • Dahl U, Sjodin A, Larue L, Radice GL, Cajander S, Takeichi M, Kemler R, Semb H. Genetic dissection of cadherin function during nephrogenesis. Mol Cell Biol 2002; 22:1474-87; PMID:11839813; http://dx.doi.org/10.1128/MCB.22.5.1474-1487.2002
  • Goto S, Yaoita E, Matsunami H, Kondo D, Yamamoto T, Kawasaki K, Arakawa M, Kihara I. Involvement of R-cadherin in the early stage of glomerulogenesis. J Am Soc Nephrol 1998; 9:1234-41; PMID:9644633
  • Maeda M, Johnson E, Mandal SH, Lawson KR, Keim SA, Svoboda RA, Caplan S, Wahl JK 3rd, Wheelock MJ, Johnson KR. Expression of inappropriate cadherins by epithelial tumor cells promotes endocytosis and degradation of E-cadherin via competition for p120(ctn). Oncogene 2006; 25:4595-604; PMID:16786001; http://dx.doi.org/10.1038/sj.onc.1209396
  • Miotto E, Sabbioni S, Veronese A, Calin GA, Gullini S, Liboni A, Gramantieri L, Bolondi L, Ferrazzi E, Gafà R, et al. Frequent aberrant methylation of the CDH4 gene promoter in human colorectal and gastric cancer. Cancer Res 2004; 64:8156-9; PMID:15548679; http://dx.doi.org/10.1158/0008-5472.CAN-04-3000
  • Kotelevets L, van Hengel J, Bruyneel E, Mareel M, van Roy F, Chastre E. Implication of the MAGI-1b/PTEN signalosome in stabilization of adherens junctions and suppression of invasiveness. FASEB J 2005; 19:115-7; PMID:15629897
  • Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012; 13:251-62; PMID:22436748; http://dx.doi.org/10.1038/nrm3311
  • Liang X, Wang P, Gao Q, Tao X. Exogenous activation of LKB1/AMPK signaling induces G(1) arrest in cells with endogenous LKB1 expression. Mol Med Rep 2014; 9:1019-24; PMID:24469340
  • Sebbagh M, Santoni MJ, Hall B, Borg JP, Schwartz MA. Regulation of LKB1/STRAD localization and function by E-cadherin. Curr Biol 2009; 19:37-42; PMID:19110428; http://dx.doi.org/10.1016/j.cub.2008.11.033
  • Partanen JI, Tervonen TA, Myllynen M, Lind E, Imai M, Katajisto P, Dijkgraaf GJ, Kovanen PE, Mäkelä TP, Werb Z, et al. Tumor suppressor function of Liver kinase B1 (Lkb1) is linked to regulation of epithelial integrity. Proc Natl Acad Sci U S A 2012; 109:E388-97; PMID:22308451; http://dx.doi.org/10.1073/pnas.1120421109
  • Wang C, Nie Z, Zhou Z, Zhang H, Liu R, Wu J, Qin J, Ma Y, Chen L, Li S, et al. The interplay between TEAD4 and KLF5 promotes breast cancer partially through inhibiting the transcription of p27Kip1. Oncotarget 2015; 6:17685-17697; PMID:25970772.
  • Hong F, Larrea MD, Doughty C, Kwiatkowski DJ, Squillace R, Slingerland JM. mTOR-raptor binds and activates SGK1 to regulate p27 phosphorylation. Mol Cell 2008; 30:701-11; PMID:18570873; http://dx.doi.org/10.1016/j.molcel.2008.04.027
  • Leontieva OV, Demidenko ZN, Blagosklonny MV. Contact inhibition and high cell density deactivate the mammalian target of rapamycin pathway, thus suppressing the senescence program. Proc Natl Acad Sci U S A 2014; 111:8832-7; PMID:24889617; http://dx.doi.org/10.1073/pnas.1405723111
  • Zhao H, Faltermeier CM, Mendelsohn L, Porter PL, Clurman BE, Roberts JM. Mislocalization of p27 to the cytoplasm of breast cancer cells confers resistance to anti-HER2 targeted therapy. Oncotarget 2014; 5:12704-14; PMID:25587029
  • Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 2011; 25:1895-908; PMID:21937710; http://dx.doi.org/10.1101/gad.17420111

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.