NHERF1 acts as a molecular switch to program metastatic behavior and organotropism via its PDZ domains

Molecular Biology of the Cell

Volumn 23, Issue 11, 2012, Pages 2028-2040

  Cardone, Rosa Angela ^a   Greco, Maria Raffaella ^a   Capulli, Mattia ^b   Weinman, Edward J ^c   Busco, Giovanni ^a   Bellizzi, Antonia ^c   Casavola, Valeria ^a   Antelmi, Ester ^a   Ambruosi, Barbara ^a   Dell'Aquila, Maria Elena ^a   Paradiso, Angelo ^d   Teti, Anna ^b   Rucci, Nadia ^b   Reshkin, Stephan Joel ^a  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF L'AQUILA   (Italy)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d NATIONAL CANCER INSTITUTE GIOVANNI PAOLO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PDZ PROTEIN; SODIUM PROTON EXCHANGE PROTEIN; SODIUM PROTON EXCHANGER REGULATORY FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL; CELL STRUCTURE; FEMALE; HUMAN; HUMAN CELL; METASTASIS; MOUSE; NONHUMAN; ORGANOTROPH; PDZ DOMAIN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR GROWTH;

ANIMALS; APOPTOSIS; CELL ADHESION; CELL LINE, TUMOR; CELL PROLIFERATION; EXTRACELLULAR MATRIX; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; PDZ DOMAINS; PHOSPHOPROTEINS; PSEUDOPODIA; SODIUM-HYDROGEN ANTIPORTER; STRUCTURE-ACTIVITY RELATIONSHIP; TROPISM; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84861697780     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-11-0911     Document Type: Article

References (59)

1. Accardi R et al. (2011). E6 and E7 from human papillomavirus type 16 cooperate to target the PDZ protein Na/H exchange regulatory factor 1. J Virol 85, 8208-8216.
2. Arguello F, Baggs RB, Frantz CN (1988). A murine model of experimental metastasis to bone and bone marrow. Cancer Res 48, 6876-6881. (Pubitemid 19012221)
3. Artym VV, Matsumoto K, Mueller SC, Yamada KM (2011). Dynamic membrane remodeling at invadopodia differentiates invadopodia from podosomes. Eur J Cell Biol 90, 172-180.
4. Basbaum CB, Werb Z (1996). Focalized proteolysis: spatial and temporal regulation of extracellular matrix degradation at the cell surface. Curr Opin Cell Biol 8, 731-738. (Pubitemid 26381732)
5. Bellizzi A, Malfettone A, Cardone RA, Mangia A (2010). NHERF1/EBP50 in breast cancer: clinical perspectives. Breast Care (Basel) 5, 86-90.
6. Bianco C, Tortora G, Baldassarre G, Caputo R, Fontanini G, Chine S, Bianco AR, Ciardiello F (1997). 8-Chloro-cyclic AMP inhibits autocrine and angiogenic growth factor production in human colorectal and breast cancer. Clin Cancer Res 3, 439-448. (Pubitemid 27158069)
7. Blouw B, Seals DF, Pass I, Diaz B, Courtneidge SA (2008). A role for the podosome/invadopodia scaffold protein Tks5 in tumor growth in vivo. Eur J Cell Biol 87, 555-567.
8. Buccione R, Caldieri G, Ayala I (2009). Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Cancer Metastasis Rev 28, 137-149.
9. Buchanan CF, Szot CS, Wilson TD, Akman S, Metheny-Barlow LJ, Robertson JL, Freeman JW, Rylander MN (2011). Cross-talk between endothelial and breast cancer cells regulates reciprocal expression of angiogenic factors in vitro. J Cell Biochem 113, 1142-1151.
10. Busco G et al. (2010). NHE1 promotes invadopodial ECM proteolysis through acidification of the peri-invadopodial space. FASEB J 24, 3903-3915.
11. Cardone RA, Bellizzi A, Busco G, Weinman EJ, Dell'Aquila ME, Casavola V, Azzariti A, Mangia A, Paradiso A, Reshkin SJ (2007). The NHERF1 PDZ2 domain regulates PKA-RhoA-p38-mediated NHE1 activation and invasion in breast tumor cells. Mol Biol Cell 18, 1768-1780. (Pubitemid 46717558)
12. Chaffer CL, Weinberg RA (2011). A perspective on cancer cell metastasis. Science 331, 1559-1564.
13. Cuddy AC, Qiu C, Gerecht S (2012). Breast cancer cell-derived matrix supports vascular morphogenesis. Am J Physiol Cell Physiol 302, C1243-C1256.
14. Dai JL, Wang L, Sahin AA, Broemeling LD, Schutte M, Pan Y (2004). NHERF (Na+/H+ exchanger regulatory factor) gene mutations in human breast cancer. Oncogene 23, 8681-8687. (Pubitemid 39576475)
15. Dome B, Hendrix MJ, Paku S, Tovari J, Timar J (2007). Alternative vascularization mechanisms in cancer: pathology and therapeutic implications. Am J Pathol 170, 1-15. (Pubitemid 47339184)
16. Dunn LK, Mohammad KS, Fournier PG, McKenna CR, Davis HW, Niewolna M, Peng XH, Chirgwin JM, Guise TA (2009). Hypoxia and TGF-beta drive breast cancer bone metastases through parallel signaling pathways in tumor cells and the bone microenvironment. PLoS One 4, e6896.
17. Fan YZ, Sun W (2010). Molecular regulation of vasculogenic mimicry in tumors and potential tumor-target therapy. World J Gastrointest Surg 2, 117-127.
18. Fiebig HH, Maier A, Burger AM (2004). Clonogenic assay with established human tumour xenografts: correlation of in vitro to in vivo activity as a basis for anticancer drug discovery. Eur J Cancer 40, 802-820. (Pubitemid 38519759)
19. Firestone AJ, Chen JK (2010). Controlling destiny through chemistry: small-molecule regulators of cell fate. ACS Chem Biol 5, 15-34.
20. Fouassier L, Nichols MT, Gidey E, McWilliams RR, Robin H, Finnigan C, Howell KE, Housset C, Doctor RB (2005). Protein kinase C regulates the phosphorylation and oligomerization of ERM binding phosphoprotein 50. Exp Cell Res 306, 264-273. (Pubitemid 40692789)
21. Garbett D, LaLonde DP, Bretscher A (2010). The scaffolding protein EBP50 regulates microvillar assembly in a phosphorylation-dependent manner. J Cell Biol 191, 397-413.
22. Geiger TR, Peeper DS (2009). Metastasis mechanisms. Biochim Biophys Acta 1796, 293-308.
23. Georgescu MM, Morales FC, Molina JR, Hayashi Y (2008). Roles of NHERF1/EBP50 in cancer. Curr Mol Med 8, 459-468.
24. Gimona M, Buccione R, Courtneidge SA, Linder S (2008). Assembly and biological role of podosomes and invadopodia. Curr Opin Cell Biol 20, 235-241.
25. Gupta GP, Massague J (2006). Cancer metastasis: building a framework. Cell 127, 679-695. (Pubitemid 44781029)
26. Hall RA, Spurney RF, Premont RT, Rahman N, Blitzer JT, Pitcher JA, Lefkowitz RJ (1999). G protein-coupled receptor kinase 6A phosphorylates the Na(+)/H(+) exchanger regulatory factor via a PDZ domain-mediated interaction. J Biol Chem 274, 24328-24334.
27. Hayashi Y, Molina JR, Hamilton SR, Georgescu MM (2010). NHERF1/EBP50 is a new marker in colorectal cancer. Neoplasia 12, 1013-1022.
28. He J, Lau AG, Yaffe MB, Hall RA (2001). Phosphorylation and cell cycle-dependent regulation of Na+/H+ exchanger regulatory factor-1 by Cdc2 kinase. J Biol Chem 276, 41559-41565.
29. Hunter KW, Alsarraj J (2009). Gene expression profiles and breast cancer metastasis: a genetic perspective. Clin Exp Metastasis 26, 497-503.
30. Jin J, Xie X, Chen C, Park JG, Stark C, James DA, Olhovsky M, Linding R, Mao Y, Pawson T (2009). Eukaryotic protein domains as functional units of cellular evolution. Sci Signal 2, ra76.
31. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J (2003). A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549. (Pubitemid 36808649)
32. Karn T et al. (2011). Gene expression profiling of luminal B breast cancers reveals NHERF1 as a new marker of endocrine resistance. Breast Cancer Res Treat 130, 409-420.
33. Kislin KL, McDonough WS, Eschbacher JM, Armstrong BA, Berens ME (2009). NHERF-1: modulator of glioblastoma cell migration and invasion. Neoplasia 11, 377-387.
34. Kreimann EL, Morales FC, de Orbeta-Cruz J, Takahashi Y, Adams H, Liu TJ, McCrea PD, Georgescu MM (2007). Cortical stabilization of beta-catenin contributes to NHERF1/EBP50 tumor suppressor function. Oncogene 26, 5290-5299. (Pubitemid 47237631)
35. Li J, Poulikakos PI, Dai Z, Testa JR, Callaway D (2007). Protein kinase C phosphorylation disrupts Na+/H+ exchanger regulatory factor 1 autoinhibition and promotes cystic fibrosis transmembrane conductance regulator macromolecular assembly. J Biol Chem 282, 27086-27099. (Pubitemid 47501969)
36. Mamonova T, Kurnikova M, Friedman PA (2012). Structural basis for NHERF1 PDZ domain binding. Biochemistry 51, 3110-3120.
37. Mayasundari A, Ferreira AM, He L, Mahindroo N, Bashford D, Fujii N (2008). Rational design of the first small-molecule antagonists of NHERF1/EBP50 PDZ domains. Bioorg Med Chem Lett 18, 942-945. (Pubitemid 351179356)
38. Minn AJ et al. (2007). Lung metastasis genes couple breast tumor size and metastatic spread. Proc Natl Acad Sci USA 104, 6740-6745. (Pubitemid 47175571)
39. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J (2005). Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524. (Pubitemid 41112921)
40. Molina JR, Agarwal NK, Morales FC, Hayashi Y, Aldape KD, Cote G, Georgescu MM (2012). PTEN, NHERF1 and PHLPP form a tumor suppressor network that is disabled in glioblastoma. Oncogene 31, 1264-1274.
41. Oser M, Dovas A, Cox D, Condeelis J (2011). Nck1 and Grb2 localization patterns can distinguish invadopodia from podosomes. Eur J Cell Biol 90, 181-188.
42. Ossowski L, Aguirre-Ghiso JA (2010). Dormancy of metastatic melanoma. Pigment Cell Melanoma Res 23, 41-56.
43. Pan Y, Wang L, Dai JL (2006). Suppression of breast cancer cell growth by Na+/H+ exchanger regulatory factor 1 (NHERF1). Breast Cancer Res 8, R63.
44. Raghuram V, Hormuth H, Foskett JK (2003). A kinase-regulated mechanism controls CFTR channel gating by disrupting bivalent PDZ domain interactions. Proc Natl Acad Sci USA 100, 9620-9625. (Pubitemid 37033977)
45. Rucci N, Recchia I, Angelucci A, Alamanou M, Del Fattore A, Fortunati D, Susa M, Fabbro D, Bologna M, Teti A (2006). Inhibition of protein kinase c-Src reduces the incidence of breast cancer metastases and increases survival in mice: implications for therapy. J Pharmacol Exp Ther 318, 161-172.
46. Shenolikar S, Voltz JW, Cunningham R, Weinman EJ (2004). Regulation of ion transport by the NHERF family of PDZ proteins. Physiology (Bethesda) 19, 362-369. (Pubitemid 39636084)
47. Song J, Bai J, Yang W, Gabrielson EW, Chan DW, Zhang Z (2007). Expression and clinicopathological significance of oestrogen-responsive ezrin-radixin-moesin-binding phosphoprotein 50 in breast cancer. Histopathology 51, 40-53. (Pubitemid 46976376)
48. Stemmer-Rachamimov AO, Wiederhold T, Nielsen GP, James M, Pinney-Michalowski D, Roy JE, Cohen WA, Ramesh V, Louis DN (2001). NHE-RF, a merlin-interacting protein, is primarily expressed in luminal epithelia, proliferative endometrium, and estrogen receptor-positive breast carcinomas. Am J Pathol 158, 57-62. (Pubitemid 32096471)
49. Sturge J, Caley MP, Waxman J (2011). Bone metastasis in prostate cancer: emerging therapeutic strategies. Nat Rev Clin Oncol 8, 357-368.
50. Stylli SS, Stacey TT, Verhagen AM, Xu SS, Pass I, Courtneidge SA, Lock P (2009). Nck adaptor proteins link Tks5 to invadopodia actin regulation and ECM degradation. J Cell Sci 122, 2727-2740.
51. Tabrizi AD, Kalloger SE, Kobel M, Cipollone J, Roskelley CD, Mehl E, Gilks CB (2010). Primary ovarian mucinous carcinoma of intestinal type: significance of pattern of invasion and immunohistochemical expression profile in a series of 31 cases. Int J Gynecol Pathol 29, 99-107.
52. van der Schaft DW, Seftor RE, Seftor EA, Hess AR, Gruman LM, Kirschmann DA, Yokoyama Y, Griffioen AW, Hendrix MJ (2004). Effects of angiogenesis inhibitors on vascular network formation by human endothelial and melanoma cells. J Natl Cancer Inst 96, 1473-1477. (Pubitemid 39429672)
53. Voltz JW, Brush M, Sikes S, Steplock D, Weinman EJ, Shenolikar S (2007). Phosphorylation of PDZ1 domain attenuates NHERF-1 binding to cellular targets. J Biol Chem 282, 33879-33887. (Pubitemid 350159561)
54. Weinman EJ, Biswas RS, Peng Q, Shen L, Turner CL, Xiaofei E, Steplock D, Shenolikar S, Cunningham R (2007). Parathyroid hormone inhibits renal phosphate transport by phosphorylation of serine 77 of sodium-hydrogen exchanger regulatory factor-1. J Clin Invest. 117, 3412-3420. (Pubitemid 350103365)
55. Weinman EJ, Wang Y, Wang F, Greer C, Steplock D, Shenolikar S (2003). A C-terminal PDZ motif in NHE3 binds NHERF-1 and enhances cAMP inhibition of sodium-hydrogen exchange. Biochemistry 42, 12662-12668. (Pubitemid 37337557)
56. Wheeler DS, Barrick SR, Grubisha MJ, Brufsky AM, Friedman PA, Romero G (2011). Direct interaction between NHERF1 and Frizzled regulates beta-catenin signaling. Oncogene 30, 32-42.
57. Yoneda T, Sasaki A, Dunstan C, Williams PJ, Bauss F, De Clerck YA, Mundy GR (1997). Inhibition of osteolytic bone metastasis of breast cancer by combined treatment with the bisphosphonate ibandronate and tissue inhibitor of the matrix metalloproteinase-2. J Clin Invest 99, 2509-2517. (Pubitemid 27227730)
58. Yoshio T, Morita T, Kimura Y, Tsujii M, Hayashi N, Sobue K (2007). Caldesmon suppresses cancer cell invasion by regulating podosome/invadopodium formation. FEBS Lett 581, 3777-3782. (Pubitemid 47102304)
59. Zheng JF, Sun LC, Liu H, Huang Y, Li Y, He J (2010). EBP50 exerts tumor suppressor activity by promoting cell apoptosis and retarding extracellular signal-regulated kinase activity. Amino Acids 38, 1261-1268.