Targeting the WASF3-CYFIP1 complex using stapled peptides suppresses cancer cell invasion

Cancer Research

Volumn 76, Issue 4, 2016, Pages 965-973

  Teng, Yong ^a   Bahassan, Abdulaziz ^a   Dong, Dayong ^a,c   Hanold, Laura E ^b   Ren, Xiaoou ^a   Kennedy, Eileen J ^b   Cowell, John K ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; CYFIP1 PROTEIN; GELATINASE B; METASTIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PEPTIDE; PEPTIDES AND PROTEINS; RAC1 PROTEIN; RAC2 PROTEIN; SCRAMBLED 1 PEPTIDE; SCRAMBLED 2 PEPTIDE; UNCLASSIFIED DRUG; WASF HELIX MIMIC 1; WASF HELIX MIMIC 2; WASF1 PROTEIN; WASF2 PROTEIN; WASF3 PROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN;

ALPHA HELIX; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER CELL LINE; CANCER INHIBITION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; COMPLEX FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYSTALLOGRAPHY; DOWN REGULATION; DRUG DESIGN; DRUG MECHANISM; DRUG TARGETING; ENZYME RELEASE; ENZYME REPRESSION; GENE SILENCING; IN VITRO STUDY; METASTASIS INHIBITION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROSTATE CANCER CELL LINE; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TUMOR INVASION; CELL MOTION; GENETICS; HUMAN; METABOLISM; METASTASIS; SIGNAL TRANSDUCTION;

CELL MOVEMENT; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PEPTIDES; SIGNAL TRANSDUCTION; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

EID: 84960469379     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-1680     Document Type: Article

References (39)

1. Sossey-Alaoui K, Su G, Malaj E, Roe B, Cowell JK. WAVE3, an actinpolymerization gene, is truncated and inactivated as a result of a constitutional t(1;13)(q21;q12) chromosome translocation in a patient with ganglioneuroblastoma. Oncogene 2002;21:5967-74.
2. Rotty JD, Wu C, Bear JE. New insights into the regulation and cellular functions of the ARP2/3 complex. Nat Rev Mol Cell Biol 2013;14:7-12.
3. Kurisu S, Takenawa T. WASP and WAVE family proteins: friends or foes in cancer invasion? Cancer Sci 2010;101:2093-104.
4. Mendoza MC. Phosphoregulation of the WAVE regulatory complex and signal integration. Semin Cell Dev Biol 2013;24:272-9.
5. Sossey-Alaoui K, Safina A, Li X, Vaughan MM, Hicks DG, Bakin AV, et al. Down-regulation of WAVE3, ametastasis promoter gene, inhibits invasion and metastasis of breast cancer cells. Am J Pathol 2007;170:211-21.
6. Chen Z, Borek D, Padrick SB, Gomez TS, Metlagel Z, Ismail AM, et al. Structure and control of the actin regulatory WAVE complex. Nature 2010;468:533-8.
7. Chen B, Brinkmann K, Chen Z, Pak CW, Liao Y, Shi S, et al. The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 2014;156:195-207.
8. Kulkarni S, Augoff K, Rivera L, McCue B, Khoury T, Groman A, et al. Increased expression levels of WAVE3 are associated with the progression and metastasis of triple negative breast cancer. PLoS One 2012;7: e42895.
9. Teng Y, Ren M, Cheney R, Sharma S, Cowell JK. Inactivation of the WASF3 gene in prostate cancer cells leads to suppression of tumorigenicity and metastases. Br J Cancer 2010;103:1066-75.
10. Teng Y, Mei Y, Hawthorn LA, Cowell JK. WASF3 regulates miR-200 inactivation by ZEB1 through suppression of KISS1 leading to increased invasiveness in breast cancer cells. Oncogene 2014;33:203-11.
11. Teng Y, LiuM, Cowell JK. Functional interrelationship between the WASF3 and KISS1 metastasis-associated genes in breast cancer cells. Int J Cancer 2011;129:2825-35.
12. Teng Y, Ross JL, Cowell JK. The involvement of JAK-STAT3 in cell motility, invasion, and metastasis. JAKSTAT 2014;3:e28086.
13. Sossey-Alaoui K, Li X, Cowell JK. c-ABL-mediated phosphorylation of WAVE3 is required for lamellipodia formation and cell migration. J Biol Chem 2007;82:26257-65.
14. Ghoshal P, Teng Y, Lesoon L, Cowell JK. HIF1A induces expression of the WASF3 metastasis associated gene under hypoxic conditions. Int J Cancer 2012;131:E905-15.
15. Teng Y, Ngoka L, Mei Y, Lesoon L, Cowell JK. HSP90 and HSP70 are essential for stabilization and activation of the WASF3 metastasis promoting protein. J Biol Chem 2012;287:10051-9.
16. Teng Y, Ghoshal P, Ngoka L, Mei Y, Cowell JK. Critical role of the WASF3 gene in JAK2/STAT3 regulation of cancer cell invasion. Carcinogenesis 2013;4:1994-9.
17. Teng Y, Ren X, Li H, Shull A, Kim J, Cowell JK. Mitochondrial ATAD3A combines with GRP78 to regulate the WASF3 metastasis-promoting protein. Oncogene 2015 Mar 30. [Epub ahead of print].
18. Schafmeister CE, Po J, Verdine GL. An all-hydrocarbon crosslinking system for enhancing the helicity and metabolic stability of peptides. J Am Chem Soc 2000;122:5891-2.
19. Blackwell HE, Sadowsky JD, Howard RJ, Sampson JN, Chao JA, Steinmetz WE, et al. Ring-closing metathesis of olefinic peptides: design, synthesis, and structural characterization ofmacrocyclic helical peptides. J Org Chem 2001;66:5291-302.
20. Walensky LD. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 2004;305:1466-70.
21. Higueruelo AP, Jubb H, Blundell TL. Protein-protein interactions as druggable targets: recent technological advances. Curr Opin Pharmacol 2013;13:791-6.
22. Verdine GL, Walensky LD. The challenge of drugging undruggable targets in cancer: lessons learned from targeting BCL-2 family members. Clin Cancer Res 2007;13:7264-70.
23. Wittrup KD, Verdine GL. Protein engineering for therapeutics, part B. Preface. Methods Enzymol 2012;503:xiii-xiv.
24. Chang YS,Graves B, Guerlavais V, Tovar C, Packman K, To KH, et al. Stapled a-helical peptide drug development: a potent dual inhibitor ofMDM2and MDMX for p53-dependent cancer therapy. Proc Natl Acad Sci U S A 2013;110:E3445-54.
25. Grigoryev Y. Stapled peptide to enter human testing, but affinity questions remain. Nat Med 2013;19:120.
26. Cromm PM, Spiegel J, Grossmann TN. Hydrocarbon stapled peptides as modulators of biological function. ACS Chem Biol 2015; 10:1362-75.
27. Wang Y, Ho TG, Bertinetti D, Neddermann M, Franz E, Mo GC, et al. Isoform-selective disruption of AKAP-localized PKA using hydrocarbon stapled peptides. ACS Chem Biol 2014;9:635-42.
28. Kunda P, Craig G, Dominguez V, Baum B. Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actinbased protrusions. Curr Biol 2003;13:1867-75.
29. Innocenti M, Zucconi A, Disanza A, Frittoli E, Areces LB, Steffen A, et al. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nat Cell Biol 2004;6:319-27.
30. Sossey-Alaoui K, Ranalli TA, Li X, Cowell JK. WAVE3 promotes cell motility and invasion through the regulation of MMP-1, MMP-3 and MMP-9-expression. Exp Cell Res 2005;308:135-45.
31. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010;12:R68.
32. Steffen A, Rottner K, Ehinger J, Innocenti M, Scita G, Wehland J, et al. Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J 2004;23:749-59.
33. IsmailAM, Padrick SB, Chen B, Umetani J, Rosen MK. TheWAVEregulatory complex is inhibited. Nat Struct Mol Biol 2009;16:561-3.
34. Lebensohn AM, Kirschner MW. Activation of the WAVE complex by coincident signals controls actin assembly. Mol Cell 2009;36:512-24.
35. Takenawa T, Suetsugu S. The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 2007;8:37-48.
36. Silva JM, Ezhkova E, Silva J, Heart S, Castillo M, Campos Y, et al. Cyfip1 is a putative invasion suppressor in epithelial cancers. Cell 2009;137:1047-61.
37. Chu Q, Moellering R, Hilinski G, Kim Y, Grossmann T, Johannes T, et al. Towards understanding cell penetration by stapled peptides. Med Chem Commun 2015;6:111-9.
38. Suetsugu S, Yamazaki D, Kurisu S, Takenawa T.Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev Cell 2003;5:2595-609.
39. Beli P, Mascheroni D, Xu D, Innocenti M. WAVE and Arp2/3 jointly inhibit filopodium formation by entering into a complex with mDia2. Nat Cell Biol 2008;10:849-57.