Epidermal growth factor receptor ligands as new extracellular targets for the metastasis-promoting S100A4 protein

FEBS Journal

Volumn 276, Issue 20, 2009, Pages 5936-5948

  Klingelhöfer, Jörg ^a,c   Møller, Henrik D ^a   Sumer, Eren U ^a   Berg, Christian H ^a   Poulsen, Maria ^a   Kiryushko, Darya ^b   Soroka, Vladislav ^b   Ambartsumian, Noona ^a   Grigorian, Mariam ^a   Lukanidin, Eugene M ^a  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c NONE   (Denmark)

Author keywords

Amphiregulin; EGFR ligand; Phage display peptide library; Protein protein interaction; S100A4

Indexed keywords

AMPHIREGULIN; CALVASCULIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; PEPTIDE LIBRARY; PROTEIN TYROSINE KINASE INHIBITOR;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RAT; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BLOTTING, FAR-WESTERN; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CHROMATOGRAPHY, GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLYCOPROTEINS; HUMANS; IMMUNOPRECIPITATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PEPTIDE LIBRARY; PEPTIDES; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; S100 PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SURFACE PLASMON RESONANCE;

EID: 70349487749     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07274.x     Document Type: Article

References (55)

1. Gibbs FE, Barraclough R, Platt-Higgins A, Rudland PS, Wilkinson MC Parry EW (1995) Immunocytochemical distribution of the calcium-binding protein p9Ka in normal rat tissues: variation in the cellular location in different tissues. J Histochem Cytochem 43, 169 180.
2. Klingelhofer J, Ambartsumian NS Lukanidin EM (1997) Expression of the metastasis-associated mts1 gene during mouse development. Dev Dyn 210, 87 95.
3. Donato R (2003) Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60, 540 551.
4. Helfman DM, Kim EJ, Lukanidin E Grigorian M (2005) The metastasis associated protein S100A4: role in tumour progression and metastasis. Br J Cancer 92, 1955 1958.
5. Merklinger SL, Wagner RA, Spiekerkoetter E, Hinek A, Knutsen RH, Kabir MG, Desai K, Hacker S, Wang L, Cann GM et al. (2005) Increased fibulin-5 and elastin in S100A4/Mts1 mice with pulmonary hypertension. Circ Res 97, 596 604.
6. Garrett SC, Varney KM, Weber DJ Bresnick AR (2006) S100A4, a mediator of metastasis. J Biol Chem 281, 677 680.
7. Klingelhofer J, Senolt L, Baslund B, Nielsen GH, Skibshøj I, Pavelka K, Neidhart M, Gay S, Ambartsumian NS, Hansen BS et al. (2007) Up-regulation of metastasis-promoting S100A4 (Mts-1) in rheumatoid arthritis: putative involvement in the pathogenesis of rheumatoid arthritis. Arthritis Rheum 56, 779 789.
8. Grigorian M, Ambartsumian N Lukanidin E (2008) Metastasis-inducing S100A4 protein: implication in non-malignant human pathologies. Curr Mol Med 8, 492 496.
9. Kozlova EN Lukanidin E (1999) Metastasis-associated mts1 (S100A4) protein is selectively expressed in white matter astrocytes and is up-regulated after peripheral nerve or dorsal root injury. Glia 27, 249 258.
10. Schneider M, Kostin S, Strøm CC, Aplin M, Lyngbæk S, Theilade J, Grigorian M, Andersen CB, Lukanidin EM, Lerche Hansen J Sheikh SP (2007) S100A4 is upregulated in injured myocardium and promotes growth and survival of cardiac myocytes. Cardiovasc Res 75, 40 50.
11. Ninomiya I, Ohta T, Fushida S, Endo Y, Hashimoto T, Yagi M, Fujimura T, Nishimura G, Tani T, Shimizu K et al. (2001) Increased expression of S100A4 and its prognostic significance in esophageal squamous cell carcinoma. Int J Oncol 18, 715 720.
12. Yonemura Y, Endou Y, Kimura K, Fushida S, Bandou E, Taniguchi K, Kinoshita K, Ninomiya I, Sugiyama K, Heizmann CW et al. (2000) Inverse expression of S100A4 and E-cadherin is associated with metastatic potential in gastric cancer. Clin Cancer Res 6, 4234 4242.
13. Gupta S, Hussain T, MacLennan GT, Fu P, Patel J Mukhtar H (2003) Differential expression of S100A2 and S100A4 during progression of human prostate adenocarcinoma. J Clin Oncol 21, 106 112.
14. Davies BR, O'Donnell M, Durkan GC, Rudland PS, Barraclough R, Neal DE Mellon JK (2002) Expression of S100A4 protein is associated with metastasis and reduced survival in human bladder cancer. J Pathol 196, 292 299.
15. Andersen K, Nesland JM, Holm R, Florenes VA, Fodstad O Maelandsmo GM (2004) Expression of S100A4 combined with reduced E-cadherin expression predicts patient outcome in malignant melanoma. Mod Pathol 17, 990 997.
16. Rudland PS, Platt-Higgins A, Renshaw C, West CR, Winstanley JH, Robertson L Barraclough R (2000) Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res 60, 1595 1603. (Pubitemid 30183430)
17. Zou M, Al-Baradie RS, Al-Hindi H, Farid NR Shi Y (2005) S100A4 (Mts1) gene overexpression is associated with invasion and metastasis of papillary thyroid carcinoma. Br J Cancer 93, 1277 1284.
18. Kriajevska MV, Cardenas MN, Grigorian MS, Ambartsumian NS, Georgiev GP Lukanidin EM (1994) Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene. J Biol Chem 269, 19679 19682.
19. Takenaga K, Nakamura Y, Sakiyama S, Hasegawa Y, Sato K Endo H (1994) Binding of pEL98 protein, an S100-related calcium-binding protein, to nonmuscle tropomyosin. J Cell Biol 124, 757 768. (Pubitemid 24085784)
20. Kriajevska M, Fischer-Larsen M, Moertz E, Vorm O, Tulchinsky E, Grigorian M, Ambartsumian N Lukanidin E (2002) Liprin β1, a member of the family of LAR transmembrane tyrosine phosphatase-interacting proteins, is a new target for the metastasis-associated protein S100A4 (Mts1). J Biol Chem 277, 5229 5235.
21. Grigorian M, Andresen S, Tulchinsky EM, Kriajevska M, Carlberg C, Kruse C, Cohn MA, Ambartsumian NS, Christensen A, Selivanova G et al. (2001) Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: functional consequences of their interaction. J Biol Chem 276, 22699 22708.
22. Novitskaya V, Grigorian M, Kriajevska M, Tarabykina S, Bronstein I, Berezin V, Bock E Lukanidin E (2000) Oligomeric forms of the metastasis-related Mts1 (S100A4) protein stimulate neuronal differentiation in cultures of rat hippocampal neurons. J Biol Chem 275, 41278 41286.
23. Pedersen MV, Kohler LB, Grigorian M, Novitskaya V, Bock E, Lukanidin E Berezin V (2004) The Mts1/S100A4 protein is a neuroprotectant. J Neurosci Res 77, 777 786.
24. Stary M, Schneider M, Sheikh SP Weitzer G (2006) Parietal endoderm secreted S100A4 promotes early cardiomyogenesis in embryoid bodies. Biochem Biophys Res Commun 343, 555 563.
25. Spiekerkoetter E, Lawrie A, Merklinger S, Ambartsumian N, Lukanidin E, Schmidt AM Rabinovitch M (2005) Mts1/S100A4 stimulates human pulmonary artery smooth muscle cell migration through multiple signaling pathways. Chest 128 (6 Suppl 577S.
26. Belot N, Pochet R, Heizmann CW, Kiss R Decaestecker C (2002) Extracellular S100A4 stimulates the migration rate of astrocytic tumor cells by modifying the organization of their actin cytoskeleton. Biochim Biophys Acta 1600, 74 83.
27. Schmidt-Hansen B, Ornas D, Grigorian M, Klingelhofer J, Tulchinsky E, Lukanidin E Ambartsumian N (2004) Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene 23, 5487 5495.
28. Ambartsumian N, Klingelhofer J, Grigorian M, Christensen C, Kriajevska M, Tulchinsky E, Georgiev G, Berezin V, Bock E, Rygaard J et al. (2001) The metastasis-associated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 20, 4685 4695.
29. Pedersen KB, Andersen K, Fodstad O Maelandsmo GM (2004) Sensitization of interferon-γ induced apoptosis in human osteosarcoma cells by extracellular S100A4. BMC Cancer 4, 52.
30. 2+ signaling in neurons induced by the S100A4 protein. Mol Cell Biol 26, 3625 3638.
31. Karasseva NG, Glinsky VV, Chen NX, Komatireddy R Quinn TP (2002) Identification and characterization of peptides that bind human ErbB-2 selected from a bacteriophage display library. J Protein Chem 21, 287 296.
32. Lakshmi MS, Parker C Sherbet GV (1993) Metastasis associated MTS1 and NM23 genes affect tubulin polymerisation in B16 melanomas: a possible mechanism of their regulation of metastatic behaviour of tumours. Anticancer Res 13, 299 303.
33. Sherbet GV, Parker C, Usmani BA Lakshmi MS (1995) Epidermal growth factor receptor status correlates with cell proliferation-related 18A2/mts1 gene expression in human carcinoma cell lines. Ann NY Acad Sci 768, 272 276.
34. Mackay A, Jones C, Dexter T, Silva RL, Bulmer K, Jones A, Simpson PT, Harris RA, Jat PS, Neville AM et al. (2003) cDNA microarray analysis of genes associated with ERBB2 (HER2/neu) overexpression in human mammary luminal epithelial cells. Oncogene 22, 2680 2688.
35. Farrow B, Sugiyama Y, Chen A, Uffort E, Nealon W Mark Evers B (2004) Inflammatory mechanisms contributing to pancreatic cancer development. Ann Surg 239, 763 769. discussion 769-771.
36. Platt-Higgins AM, Renshaw CA, West CR, Winstanley JH, De Rudland Silva S, Barraclough R Rudland PS (2000) Comparison of the metastasis-inducing protein S100A4 (p9ka) with other prognostic markers in human breast cancer. Int J Cancer 89, 198 208. (Pubitemid 30185931)
37. Tarbe N, Losch S, Burtscher H, Jarsch M Weidle UH (2002) Identification of rat pancreatic carcinoma genes associated with lymphogenous metastasis. Anticancer Res 22, 2015 2027.
38. Davies MP, Rudland PS, Robertson L, Parry EW, Jolicoeur P Barraclough R (1996) Expression of the calcium-binding protein S100A4 (p9Ka) in MMTV-neu transgenic mice induces metastasis of mammary tumours. Oncogene 13, 1631 1637.
39. Marenholz I, Heizmann CW Fritz G (2004) S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 322, 1111 1122.
40. Shoyab M, McDonald VL, Bradley JG Todaro GJ (1988) Amphiregulin: a bifunctional growth-modulating glycoprotein produced by the phorbol 12-myristate 13-acetate-treated human breast adenocarcinoma cell line MCF-7. Proc Natl Acad Sci USA 85, 6528 6532.
41. Schuger L, Johnson GR, Gilbride K, Plowman GD Mandel R (1996) Amphiregulin in lung branching morphogenesis: interaction with heparan sulfate proteoglycan modulates cell proliferation. Development 122, 1759 1767.
42. Willmarth NE, Baillo A, Dziubinski ML, Wilson K, Riese DJ II. Ethier SP (2009) Altered EGFR localization and degradation in human breast cancer cells with an Amphiregulin/EGFR autocrine loop. Cell Signal 21, 212 219.
43. Cook PW, Ashton NM, Karkaria CE, Siess DC Shipley GD (1995) Differential effects of a heparin antagonist (hexadimethrine) or chlorate on amphiregulin, basic fibroblast growth factor, and heparin-binding EGF-like growth factor activity. J Cell Physiol 163, 418 429.
44. Grum-Schwensen B, Klingelhofer J, Berg CH, El-Naaman C, Grigorian M, Lukanidin E Ambartsumian N (2005) Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res 65, 3772 3780.
45. Yammani RR, Carlson CS, Bresnick AR Loeser RF (2006) Increase in production of matrix metalloproteinase 13 by human articular chondrocytes due to stimulation with S100A4: role of the receptor for advanced glycation end products. Arthritis Rheum 54, 2901 2911.
46. Levitzki A Gazit A (1995) Tyrosine kinase inhibition: an approach to drug development. Science 267, 1782 1788.
47. Oslejskova L, Grigorian M, Gay S, Neidhart M Senolt L (2008) The metastasis associated protein S100A4: a potential novel link to inflammation and consequent aggressive behaviour of rheumatoid arthritis synovial fibroblasts. Ann Rheum Dis 67, 1499 1504.
48. Cabezon T et al. (2007) Expression of S100A4 by a variety of cell types present in the tumor microenvironment of human breast cancer. Int J Cancer 121, 1433 1444.
49. Ogiso H, Ishitani R, Nureki O, Fukai S, Yamanaka M, Kim J, Saito K, Sakamoto A, Inoue M, Shirouzu M et al. (2002) Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 110, 775 787.
50. Semov A et al. (2005) Metastasis-associated protein S100A4 induces angiogenesis through interaction with annexin II and accelerated plasmin formation. J Biol Chem 280, 20833 20841.
51. Dethlefsen SM, Raab G, Moses MA, Adam RM, Klagsbrun M Freeman MR (1998) Extracellular calcium influx stimulates metalloproteinase cleavage and secretion of heparin-binding EGF-like growth factor independently of protein kinase C. J Cell Biochem 69, 143 153.
52. Horiuchi K et al. (2007) Substrate selectivity of epidermal growth factor-receptor ligand sheddases and their regulation by phorbol esters and calcium influx. Mol Biol Cell 18, 176 188.
53. Shaw SS, Schmidt AM, Banes AK, Wang X, Stern DM Marrero MB (2003) S100B-RAGE-mediated augmentation of angiotensin II-induced activation of JAK2 in vascular smooth muscle cells is dependent on PLD2. Diabetes 52, 2381 2388. (Pubitemid 37059510)
54. Weiss FU, Daub H Ullrich A (1997) Novel mechanisms of RTK signal generation. Curr Opin Genet Dev 7, 80 86.
55. Wang XT, McCullough KD, Wang XJ, Carpenter G Holbrook NJ (2001) Oxidative stress-induced phospholipase C-γ1 activation enhances cell survival. J Biol Chem 276, 28364 28371.