CIP4 promotes metastasis in triple-negative breast cancer and is associated with poor patient prognosis

Oncotarget

Volumn 6, Issue 11, 2015, Pages 9397-9408

  Cerqueira, Otto L D ^a   Truesdell, Peter ^b   Baldassarre, Tomas ^b   Vilella Arias, Santiago A ^a   Watt, Kathleen ^b   Meens, Jalna ^b   Chander, Harish ^b   Osório, Cynthia A B ^c   Soares, Fernando A ^c,d   Reis, Eduardo M ^a,d   Craig, Andrew W B ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b QUEEN S UNIVERSITY   (Canada)

^c A C CAMARGO CANCER CENTER   (Brazil)

^d Instituto Nacional de Ciencia e Tecnologia   (Brazil)

Author keywords

CIP4; Metastasis; Triple negative breast cancer

Indexed keywords

CDC42 INTERACTING PROTEIN 4; EPIDERMAL GROWTH FACTOR RECEPTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; UNCLASSIFIED DRUG; MICROTUBULE ASSOCIATED PROTEIN; MINOR HISTOCOMPATIBILITY ANTIGEN; TRIP10 PROTEIN, HUMAN;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER CELL LINE; BREAST CARCINOMA; CANCER PROGNOSIS; CANCER STAGING; CELL INVASION; CELL MOTILITY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG METASTASIS; MAJOR CLINICAL STUDY; NONHUMAN; PROTEIN EXPRESSION; RAT; TRIPLE NEGATIVE BREAST CANCER; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; CARCINOMA, DUCTAL, BREAST; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METASTASIS; MIDDLE AGED; MORTALITY; MOUSE; PATHOLOGY; PHYSIOLOGY; PROGNOSIS; TRANSGENIC MOUSE; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE; TUMOR INVASION; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; MIDDLE AGED; MINOR HISTOCOMPATIBILITY ANTIGENS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PROGNOSIS; RATS; TRIPLE NEGATIVE BREAST NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS; YOUNG ADULT;

EID: 84928719461     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3351     Document Type: Article

References (42)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Intl J Cancer. 2010; 127:2893-2917.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics. CA Cancer J Clin. 2012; 62:10-29.
3. Sotiriou C, Pusztai L. Gene-expression signatures in breast cancer. New Engl J Med. 2009; 360:790-800.
4. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011; 121:2750-2767.
5. Rakha EA, El-Sayed ME, Reis-Filho J, Ellis IO. Pathobiological aspects of basal-like breast cancer. Breast Cancer Res Treat. 2009; 113:411-422.
6. Rakha EA, Reis-Filho JS, Ellis IO. Basal-like breast cancer: a critical review. J Clin Oncol. 2008; 26:2568-2581.
7. Chambers AF, Groom AC, MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer. 2002; 2:563-572.
8. Buccione R, Caldieri G, Ayala I. Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Cancer Met Rev. 2009; 28:137-149.
9. Gligorijevic B, Wyckoff J, Yamaguchi H, Wang Y, Roussos ET, Condeelis J. N-WASP-mediated invadopodium formation is involved in intravasation and lung metastasis of mammary tumors. J Cell Sci. 2012; 125:724-734.
10. Oser M, Yamaguchi H, Mader CC, Bravo-Cordero JJ, Arias M, Chen X, Desmarais V, van Rheenen J, Koleske AJ, Condeelis J. Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J Cell Biol. 2009; 186:571-587.
11. Hu J, Mukhopadhyay A, Truesdell P, Chander H, Mukhopadhyay UK, Mak AS, Craig AW. Cdc42-interacting protein 4 is a Src substrate that regulates invadopodia and invasiveness of breast tumors by promoting MT1-MMP endocytosis. J Cell Sci. 2011; 124:1739-1751.
12. Pichot CS, Arvanitis C, Hartig SM, Jensen SA, Bechill J, Marzouk S, Yu J, Frost JA, Corey SJ. Cdc42-interacting protein 4 promotes breast cancer cell invasion and formation of invadopodia through activation of N-WASp. Cancer Res. 2010; 70:8347-8356.
13. Aspenstrom P. A Cdc42 target protein with homology to the non-kinase domain of FER has a potential role in regulating the actin cytoskeleton. Curr Biol. 1997; 7:479-487.
14. Shimada A, Niwa H, Tsujita K, Suetsugu S, Nitta K, Hanawa-Suetsugu K, Akasaka R, Nishino Y, Toyama M, Chen L, Liu ZJ, Wang BC, Yamamoto M, Terada T, Miyazawa A, Tanaka A, et al. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell. 2007; 129:761-772.
15. Frost A, Perera R, Roux A, Spasov K, Destaing O, Egelman EH, De Camilli P, Unger VM. Structural basis of membrane invagination by F-BAR domains. Cell. 2008; 132:807-817.
16. Hu J, Troglio F, Mukhopadhyay A, Everingham S, Kwok E, Scita G, Craig AW. F-BAR-containing adaptor CIP4 localizes to early endosomes and regulates Epidermal Growth Factor Receptor trafficking and downregulation. Cell Signal. 2009; 21:1686-1697.
17. Saengsawang W, Taylor KL, Lumbard DC, Mitok K, Price A, Pietila L, Gomez TM, Dent EW. CIP4 coordinates with phospholipids and actin-associated proteins to localize to the protruding edge and produce actin ribs and veils. J Cell Sci. 2013; 126:2411-2423.
18. Aspenstrom P, Richnau N, Johansson AS. The diaphanous- related formin DAAM1 collaborates with the Rho GTPases RhoA and Cdc42, CIP4 and Src in regulating cell morphogenesis and actin dynamics. Exp Cell Res. 2006; 312:2180-2194.
19. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, De Camilli P. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell. 2005; 9:791-804.
20. Roignot J, Taieb D, Suliman M, Dusetti NJ, Iovanna JL, Soubeyran P. CIP4 is a new ArgBP2 interacting protein that modulates the ArgBP2 mediated control of WAVE1 phosphorylation and cancer cell migration. Cancer Lett. 2010; 288:116-123.
21. Truesdell P, Ahn J, Chander H, Meens J, Watt K, Yang X, Craig AW. CIP4 promotes lung adenocarcinoma metastasis and is associated with poor prognosis. Oncogene. 2014; Epub Sep 1.
22. Raghu H, Sodadasu PK, Malla RR, Gondi CS, Estes N, Rao JS. Localization of uPAR and MMP-9 in lipid rafts is critical for migration, invasion and angiogenesis in human breast cancer cells. BMC Cancer. 2010; 10:647.
23. Chander H, Truesdell P, Meens J, Craig AW. Transducer of Cdc42-dependent actin assembly promotes breast cancer invasion and metastasis. Oncogene. 2013; 32:3080-3090.
24. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Lonning PE, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA. 2001; 98:10869-10874.
25. Rakha EA, Reis-Filho JS, Ellis IO. Combinatorial biomarker expression in breast cancer. Breast Cancer Res Treat. 2010; 120:293-308.
26. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MC, Nielsen TO, Moorman PG, Earp HS, et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006; 295:2492-2502.
27. O'Brien KM, Cole SR, Tse CK, Perou CM, Carey LA, Foulkes WD, Dressler LG, Geradts J, Millikan RC. Intrinsic breast tumor subtypes, race, and long-term survival in the Carolina Breast Cancer Study. Clin Cancer Res. 2010; 16:6100-6110.
28. Camp RL, Dolled-Filhart M, Rimm DL. X-tile: a new bioinformatics tool for biomarker assessment and outcomebased cut-point optimization. Clin Cancer Res. 2004; 10:7252-7259.
29. Saengsawang W, Mitok K, Viesselmann C, Pietila L, Lumbard DC, Corey SJ, Dent EW. The F-BAR protein CIP4 inhibits neurite formation by producing lamellipodial protrusions. Curr Biol. 2012; 22:494-501.
30. Rolland Y, Marighetti P, Malinverno C, Confalonieri S, Luise C, Ducano N, Palamidessi A, Bisi S, Kajiho H, Troglio F, Shcherbakova OG, Dunn AR, Oldani A, Lanzetti L, Di Fiore PP, Disanza A, et al. The CDC42-Interacting Protein 4 Controls Epithelial Cell Cohesion and Tumor Dissemination. Dev Cell. 2014; 30:553-568.
31. Livasy CA, Karaca G, Nanda R, Tretiakova MS, Olopade OI, Moore DT, Perou CM. Phenotypic evaluation of the basal-like subtype of invasive breast carcinoma. Modern Pathol. 2006; 19:264-271.
32. Lehmann BD, Pietenpol JA. Identification and use of biomarkers in treatment strategies for triple-negative breast cancer subtypes. J Pathol. 2014; 232:142-150.
33. Tsujita K, Suetsugu S, Sasaki N, Furutani M, Oikawa T, Takenawa T. Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J Cell Biol. 2006; 172:269-279.
34. Gomes LR, Terra LF, Wailemann RA, Labriola L, Sogayar MC. TGF-beta1 modulates the homeostasis between MMPs and MMP inhibitors through p38 MAPK and ERK1/2 in highly invasive breast cancer cells. BMC Cancer. 2012; 12:26.
35. Bae GY, Choi SJ, Lee JS, Jo J, Lee J, Kim J, Cha HJ. Loss of E-cadherin activates EGFR-MEK/ERK signaling, which promotes invasion via the ZEB1/MMP2 axis in non-small cell lung cancer. Oncotarget. 2013; 4:2512-2522.
36. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, Rimm DL, Wong H, Rodriguez A, Herschkowitz JI, Fan C, Zhang X, He X, Pavlick A, Gutierrez MC, Renshaw L, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA. 2009; 106:13820-13825.
37. Bai S, Zeng R, Zhou Q, Liao W, Zhang Y, Xu C, Han M, Pei G, Liu L, Liu X, Yao Y, Xu G. Cdc42-interacting protein-4 promotes TGF-Beta1-induced epithelialmesenchymal transition and extracellular matrix deposition in renal proximal tubular epithelial cells. Intl J Biol Sci. 2012; 8:859-869.
38. Dumont N, Bakin AV, Arteaga CL. Autocrine transforming growth factor-beta signaling mediates Smad-independent motility in human cancer cells. J Biol Chem. 2003; 278:3275-3285.
39. Koshkina NV, Yang G, Kleinerman ES. Inhibition of Cdc42-interacting protein 4 (CIP4) impairs osteosarcoma tumor progression. Curr Cancer Drug Targets. 2013; 13:48-56.
40. Soon L, Braet F, Condeelis J. Moving in the right direction- nanoimaging in cancer cell motility and metastasis. Microscopy Res Tech. 2007; 70:252-257.
41. Xue C, Wyckoff J, Liang F, Sidani M, Violini S, Tsai KL, Zhang ZY, Sahai E, Condeelis J, Segall JE. Epidermal growth factor receptor overexpression results in increased tumor cell motility in vivo coordinately with enhanced intravasation and metastasis. Cancer Res. 2006; 66:192-197.
42. Le Devedec SE, van Roosmalen W, Maria N, Grimbergen M, Pont C, Lalai R, van de Water B. An improved model to study tumor cell autonomous metastasis programs using MTLn3 cells and the Rag2(-/-) gammac (-/-) mouse. Clin Exp Metastasis. 2009; 26:673-684.