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Role of DDR1 in the gelatinases secretion induced by native type IV collagen in MDA-MB-231 breast cancer cells

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Abstract

Discoidin domain receptors (DDRs) are receptor tyrosine kinases that get activated by collagens in its native triple-helical form. In mammalian cells, DDR family consists of two members, namely DDR1 and DDR2, which mediates migration and proliferation of several cell types. DDR1 is activated by native type IV collagen and overexpressed in human breast cancer. Type IV collagen is the main component of basement membrane (BM), and the ability to degrade and penetrate BM is related with an increased potential for invasion and metastasis. Matrix metalloproteinases (MMPs) are a family of zinc-dependent endopeptidases that collectively are capable of degrading all components of the extracellular matrix, including the BM. In breast cancer cells, denatured type IV collagen induces MMP-9 secretion and invasion. However, the role of DDR1 in the regulation of gelatinases (MMP-2 and -9) secretion and invasion in breast cancer cells remains to be studied. We demonstrate here that native type IV collagen induces MMP-2 and -9 secretions and invasion through a DDR1 and Src-dependent pathway, together with an increase of MMP-2 and -9-cell surface levels. MMP-2 and -9 secretions require PKC kinase activity, epidermal growth factor receptor (EGFR) activation, arachidonic acid (AA) production and AA metabolites in MDA-MB-231 breast cancer cells. In summary, our data demonstrate, for the first time, that DDR1 mediates MMP-2 and -9 secretions and invasion induced by native type IV collagen in MDA-MB-231 breast cancer cells.

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References

  1. Liotta LA, Steeg PS, Stetler-Stevenson WG (1991) Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 64:327–336

    Article  PubMed  CAS  Google Scholar 

  2. Nagase H, Woessner JF Jr (1999) Matrix metalloproteinases. J Biol Chem 274:21491–21494

    Article  PubMed  CAS  Google Scholar 

  3. Stetler-Stevenson WG, Liotta LA, Kleiner DE Jr (1993) Extracellular matrix 6: role of matrix metalloproteinases in tumor invasion and metastasis. FASEB J 7:1434–1441

    PubMed  CAS  Google Scholar 

  4. Aumailley M, Gayraud B (1998) Structure and biological activity of the extracellular matrix. J Mol Med 76:253–265

    Article  PubMed  CAS  Google Scholar 

  5. Boudreau N, Sympson CJ, Werb Z, Bissell MJ (1995) Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267:891–893

    Article  PubMed  CAS  Google Scholar 

  6. Muschler J, Lochter A, Roskelley CD, Yurchenco P, Bissell MJ (1999) Division of labor among the alpha6beta4 integrin, beta1 integrins, and an E3 laminin receptor to signal morphogenesis and beta-casein expression in mammary epithelial cells. Mol Biol Cell 10:2817–2828

    PubMed  CAS  Google Scholar 

  7. Weaver VM, Lelievre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, Werb Z, Bissell MJ (2002) Beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2:205–216

    Article  PubMed  CAS  Google Scholar 

  8. Miles AJ, Skubitz AP, Furcht LT, Fields GB (1994) Promotion of cell adhesion by single-stranded and triple-helical peptide models of basement membrane collagen alpha 1(IV)531–543. Evidence for conformationally dependent and conformationally independent type IV collagen cell adhesion sites. J Biol Chem 269:30939–30945

    PubMed  CAS  Google Scholar 

  9. Vogel WF, Abdulhussein R, Ford CE (2006) Sensing extracellular matrix: an update on discoidin domain receptor function. Cell Signal 18:1108–1116

    Article  PubMed  CAS  Google Scholar 

  10. Yoshinaga IG, Vink J, Dekker SK, Mihm MC Jr, Byers HR (1993) Role of alpha 3 beta 1 and alpha 2 beta 1 integrins in melanoma cell migration. Melanoma Res 3:435–441

    Article  PubMed  CAS  Google Scholar 

  11. Alves F, Vogel W, Mossie K, Millauer B, Hofler H, Ullrich A (1995) Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 10:609–618

    PubMed  CAS  Google Scholar 

  12. Vogel W, Gish GD, Alves F, Pawson T (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1:13–23

    Article  PubMed  CAS  Google Scholar 

  13. Shrivastava A, Radziejewski C, Campbell E, Kovac L, McGlynn M, Ryan TE, Davis S, Goldfarb MP, Glass DJ, Lemke G, Yancopoulos GD (1997) An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol Cell 1:25–34

    Article  PubMed  CAS  Google Scholar 

  14. Hou G, Vogel W, Bendeck MP (2001) The discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J Clin Invest 107:727–735

    Article  PubMed  CAS  Google Scholar 

  15. Matsuyama W, Faure M, Yoshimura T (2003) Activation of discoidin domain receptor 1 facilitates the maturation of human monocyte-derived dendritic cells through the TNF receptor associated factor 6/TGF-beta-activated protein kinase 1 binding protein 1 beta/p38 alpha mitogen-activated protein kinase signaling cascade. J Immunol 171:3520–3532

    PubMed  CAS  Google Scholar 

  16. Kamohara H, Yamashiro S, Galligan C, Yoshimura T (2001) Discoidin domain receptor 1 isoform-a (DDR1alpha) promotes migration of leukocytes in three-dimensional collagen lattices. FASEB J 15:2724–2726

    PubMed  CAS  Google Scholar 

  17. Koo DH, McFadden C, Huang Y, Abdulhussein R, Friese-Hamim M, Vogel WF (2006) Pinpointing phosphotyrosine-dependent interactions downstream of the collagen receptor DDR1. FEBS Lett 580:15–22

    Article  PubMed  CAS  Google Scholar 

  18. Matsuyama W, Kamohara H, Galligan C, Faure M, Yoshimura T (2003) Interaction of discoidin domain receptor 1 isoform b (DDR1b) with collagen activates p38 mitogen-activated protein kinase and promotes differentiation of macrophages. FASEB J 17:1286–1288

    PubMed  CAS  Google Scholar 

  19. Matsuyama W, Wang L, Farrar WL, Faure M, Yoshimura T (2004) Activation of discoidin domain receptor 1 isoform b with collagen up-regulates chemokine production in human macrophages: role of p38 mitogen-activated protein kinase and NF-kappa B. J Immunol 172:2332–2340

    PubMed  CAS  Google Scholar 

  20. Lu KK, Trcka D, Bendeck MP (2010) Collagen stimulates discoidin domain receptor 1-mediated migration of smooth muscle cells through Src. Cardiovasc Pathol doi:10.1016/j.carpath.2009.12.006

  21. Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2:161–174

    Article  PubMed  CAS  Google Scholar 

  22. Coussens LM, Fingleton B, Matrisian LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295:2387–2392

    Article  PubMed  CAS  Google Scholar 

  23. Curran S, Murray GI (2000) Matrix metalloproteinases: molecular aspects of their roles in tumour invasion and metastasis. Eur J Cancer 36:1621–1630

    Article  PubMed  CAS  Google Scholar 

  24. Folgueras AR, Pendas AM, Sanchez LM, Lopez-Otin C (2004) Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. Int J Dev Biol 48:411–424

    Article  PubMed  CAS  Google Scholar 

  25. McCawley LJ, Matrisian LM (2000) Matrix metalloproteinases: multifunctional contributors to tumor progression. Mol Med Today 6:149–156

    Article  PubMed  CAS  Google Scholar 

  26. Robledo T, Arriaga-Pizano L, Lopez-Perez M, Salazar EP (2005) Type IV collagen induces STAT5 activation in MCF7 human breast cancer cells. Matrix Biol 24:469–477

    Article  PubMed  CAS  Google Scholar 

  27. Santoro SA, Cunningham LW (1982) Platelet-collagen adhesion. Methods Enzymol 82(Pt A):509–513

    Google Scholar 

  28. Munoz ML, Calderon J, Rojkind M (1982) The collagenase of Entamoeba histolytica. J Exp Med 155:42–51

    Article  PubMed  CAS  Google Scholar 

  29. Timpl R, Oberbaumer I, von der Mark H, Bode W, Wick G, Weber S, Engel J (1985) Structure and biology of the globular domain of basement membrane type IV collagen. Ann N Y Acad Sci 460:58–72

    Article  PubMed  CAS  Google Scholar 

  30. Friedrichson T, Kurzchalia TV (1998) Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394:802–805

    Article  PubMed  CAS  Google Scholar 

  31. Cortes-Reynosa P, Robledo T, Macias-Silva M, Wu SV, Salazar EP (2008) Src kinase regulates metalloproteinase-9 secretion induced by type IV collagen in MCF-7 human breast cancer cells. Matrix Biol 27:220–231

    Article  PubMed  CAS  Google Scholar 

  32. Vogel W (1999) Discoidin domain receptors: structural relations and functional implications. FASEB J 13(Suppl):S77–S782

    PubMed  CAS  Google Scholar 

  33. Park HS, Kim KR, Lee HJ, Choi HN, Kim DK, Kim BT, Moon WS (2007) Overexpression of discoidin domain receptor 1 increases the migration and invasion of hepatocellular carcinoma cells in association with matrix metalloproteinase. Oncol Rep 18:1435–1441

    PubMed  CAS  Google Scholar 

  34. Ke Z, Lin H, Fan Z, Cai TQ, Kaplan RA, Ma C, Bower KA, Shi X, Luo J (2006) MMP-2 mediates ethanol-induced invasion of mammary epithelial cells over-expressing ErbB2. Int J Cancer 119:8–16

    Article  PubMed  CAS  Google Scholar 

  35. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J Biol Chem 271:695–701

    Article  PubMed  CAS  Google Scholar 

  36. Liu JF, Crepin M, Liu JM, Barritault D, Ledoux D (2002) FGF-2 and TPA induce matrix metalloproteinase-9 secretion in MCF-7 cells through PKC activation of the Ras/ERK pathway. Biochem Biophys Res Commun 293:1174–1182

    Article  PubMed  CAS  Google Scholar 

  37. Yao J, Xiong S, Klos K, Nguyen N, Grijalva R, Li P, Yu D (2001) Multiple signaling pathways involved in activation of matrix metalloproteinase-9 (MMP-9) by heregulin-beta1 in human breast cancer cells. Oncogene 20:8066–8074

    Article  PubMed  CAS  Google Scholar 

  38. Soto-Guzman A, Navarro-Tito N, Castro-Sanchez L, Martinez-Orozco R, Salazar EP (2010) Oleic acid promotes MMP-9 secretion and invasion in breast cancer cells. Clin Exp Metastasis 27:505–515

    Article  PubMed  CAS  Google Scholar 

  39. Toullec D, Pianetti P, Coste H, Bellevergue P, Grand-Perret T, Ajakane M, Baudet V, Boissin P, Boursier E, Loriolle F (1991) The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem 266:15771–15781

    PubMed  CAS  Google Scholar 

  40. Ward WH, Cook PN, Slater AM, Davies DH, Holdgate GA, Green LR (1994) Epidermal growth factor receptor tyrosine kinase. Investigation of catalytic mechanism, structure-based searching and discovery of a potent inhibitor. Biochem Pharmacol 48:659–666

    Article  PubMed  CAS  Google Scholar 

  41. Koontongkaew S, Monthanapisut P, Saensuk T (2010) Inhibition of arachidonic acid metabolism decreases tumor cell invasion and matrix metalloproteinase expression. Prostaglandins Other Lipid Mediat 93:100–108

    Article  PubMed  CAS  Google Scholar 

  42. Solakivi T, Kunnas T, Karkkainen S, Jaakkola O, Nikkari ST (2009) Arachidonic acid increases matrix metalloproteinase 9 secretion and expression in human monocytic MonoMac 6 cells. Lipids Health Dis 8:11

    Article  PubMed  CAS  Google Scholar 

  43. Chau LY, Tai HH (1981) Release of arachidonate from diglyceride in human platelets requires the sequential action of a diglyceride lipase and a monoglyceride lipase. Biochem Biophys Res Commun 100:1688–1695

    Article  PubMed  CAS  Google Scholar 

  44. Dessen A (2000) Structure and mechanism of human cytosolic phospholipase A(2). Biochim Biophys Acta 1488:40–47

    PubMed  CAS  Google Scholar 

  45. Harizi H, Corcuff JB, Gualde N (2008) Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology. Trends Mol Med 14:461–469

    Article  PubMed  CAS  Google Scholar 

  46. Rebecchi MJ, Pentyala SN (2000) Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev 80:1291–1335

    PubMed  CAS  Google Scholar 

  47. Seno K, Okuno T, Nishi K, Murakami Y, Watanabe F, Matsuura T, Wada M, Fujii Y, Yamada M, Ogawa T, Okada T, Hashizume H, Kii M, Hara S, Hagishita S, Nakamoto S, Yamada K, Chikazawa Y, Ueno M, Teshirogi I, Ono T, Ohtani M (2000) Pyrrolidine inhibitors of human cytosolic phospholipase A(2). J Med Chem 43:1041–1044

    Article  PubMed  CAS  Google Scholar 

  48. Tatrai A, Lee SK, Stern PH (1994) U-73122, a phospholipase C antagonist, inhibits effects of endothelin-1 and parathyroid hormone on signal transduction in UMR-106 osteoblastic cells. Biochim Biophys Acta 1224:575–582

    Article  PubMed  Google Scholar 

  49. Nony PA, Kennett SB, Glasgow WC, Olden K, Roberts JD (2005) 15S-Lipoxygenase-2 mediates arachidonic acid-stimulated adhesion of human breast carcinoma cells through the activation of TAK1, MKK6, and p38 MAPK. J Biol Chem 280:31413–31419

    Article  PubMed  CAS  Google Scholar 

  50. Park H, Aiyar SE, Fan P, Wang J, Yue W, Okouneva T, Cox C, Jordan MA, Demers L, Cho H, Kim S, Song RX, Santen RJ (2007) Effects of tetramethoxystilbene on hormone-resistant breast cancer cells: biological and biochemical mechanisms of action. Cancer Res 67:5717–5726

    Article  PubMed  CAS  Google Scholar 

  51. Seibert K, Masferrer JL, Needleman P, Salvemini D (1996) Pharmacological manipulation of cyclo-oxygenase-2 in the inflamed hydronephrotic kidney. Br J Pharmacol 117:1016–1020

    PubMed  CAS  Google Scholar 

  52. Liotta LA, Kohn EC (2001) The microenvironment of the tumour-host interface. Nature 411:375–379

    Article  PubMed  CAS  Google Scholar 

  53. McDonald JA (1988) Extracellular matrix assembly. Annu Rev Cell Biol 4:183–207

    Article  PubMed  CAS  Google Scholar 

  54. McClay DR, Ettensohn CA (1987) Cell adhesion in morphogenesis. Annu Rev Cell Biol 3:319–345

    Article  PubMed  CAS  Google Scholar 

  55. Alford D, Taylor-Papadimitriou J (1996) Cell adhesion molecules in the normal and cancerous mammary gland. J Mammary Gland Biol Neoplasia 1:207–218

    Article  PubMed  CAS  Google Scholar 

  56. Owens LV, Xu L, Craven RJ, Dent GA, Weiner TM, Kornberg L, Liu ET, Cance WG (1995) Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res 55:2752–2755

    PubMed  CAS  Google Scholar 

  57. Schaller MD (2001) Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim Biophys Acta 1540:1–21

    Article  PubMed  CAS  Google Scholar 

  58. Castro-Sanchez L, Soto-Guzman A, Navarro-Tito N, Martinez-Orozco R, Salazar EP (2010) Native type IV collagen induces cell migration through a CD9 and DDR1-dependent pathway in MDA-MB-231 breast cancer cells. Eur J Cell Biol 89:843–852

    Article  PubMed  CAS  Google Scholar 

  59. Vogel WF, Aszodi A, Alves F, Pawson T (2001) Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol Cell Biol 21:2906–2917

    Article  PubMed  CAS  Google Scholar 

  60. Dejmek J, Leandersson K, Manjer J, Bjartell A, Emdin SO, Vogel WF, Landberg G, Andersson T (2005) Expression and signaling activity of Wnt-5a/discoidin domain receptor-1 and Syk plays distinct but decisive roles in breast cancer patient survival. Clin Cancer Res 11:520–528

    PubMed  CAS  Google Scholar 

  61. Barker KT, Martindale JE, Mitchell PJ, Kamalati T, Page MJ, Phippard DJ, Dale TC, Gusterson BA, Crompton MR (1995) Expression patterns of the novel receptor-like tyrosine kinase, DDR, in human breast tumours. Oncogene 10:569–575

    PubMed  CAS  Google Scholar 

  62. Mihai C, Chotani M, Elton TS, Agarwal G (2009) Mapping of DDR1 distribution and oligomerization on the cell surface by FRET microscopy. J Mol Biol 385:432–445

    Article  PubMed  CAS  Google Scholar 

  63. Bourboulia D, Stetler-Stevenson WG (2010) Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): Positive and negative regulators in tumor cell adhesion. Semin Cancer Biol 20:161–168

    Article  PubMed  CAS  Google Scholar 

  64. Duffy MJ, Maguire TM, Hill A, McDermott E, O’Higgins N (2000) Metalloproteinases: role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res 2:252–257

    Article  PubMed  CAS  Google Scholar 

  65. Liotta LA, Tryggvason K, Garbisa S, Hart I, Foltz CM, Shafie S (1980) Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284:67–68

    Article  PubMed  CAS  Google Scholar 

  66. Xu J, Rodriguez D, Petitclerc E, Kim JJ, Hangai M, Moon YS, Davis GE, Brooks PC (2001) Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J Cell Biol 154:1069–1079

    Article  PubMed  CAS  Google Scholar 

  67. Hou G, Vogel WF, Bendeck MP (2002) Tyrosine kinase activity of discoidin domain receptor 1 is necessary for smooth muscle cell migration and matrix metalloproteinase expression. Circ Res 90:1147–1149

    Article  PubMed  CAS  Google Scholar 

  68. Jezierska A, Motyl T (2009) Matrix metalloproteinase-2 involvement in breast cancer progression: a mini-review. Med Sci Monit 15:RA32–RA40

    PubMed  CAS  Google Scholar 

  69. Brooks PC, Stromblad S, Sanders LC, von Schalscha TL, Aimes RT, Stetler-Stevenson WG, Quigley JP, Cheresh DA (1996) Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85:683–693

    Article  PubMed  CAS  Google Scholar 

  70. Rolli M, Fransvea E, Pilch J, Saven A, Felding-Habermann B (2003) Activated integrin alphavbeta3 cooperates with metalloproteinase MMP-9 in regulating migration of metastatic breast cancer cells. Proc Natl Acad Sci USA 100:9482–9487

    Article  PubMed  CAS  Google Scholar 

  71. Seftor RE, Seftor EA, Stetler-Stevenson WG, Hendrix MJ (1993) The 72 kDa type IV collagenase is modulated via differential expression of alpha v beta 3 and alpha 5 beta 1 integrins during human melanoma cell invasion. Cancer Res 53:3411–3415

    PubMed  CAS  Google Scholar 

  72. Iwata H, Kobayashi S, Iwase H, Masaoka A, Fujimoto N, Okada Y (1996) Production of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human breast carcinomas. Jpn J Cancer Res 87:602–611

    PubMed  CAS  Google Scholar 

  73. Benaud C, Dickson RB, Thompson EW (1998) Roles of the matrix metalloproteinases in mammary gland development and cancer. Breast Cancer Res Treat 50:97–116

    Article  PubMed  CAS  Google Scholar 

  74. Curran S, Murray GI (1999) Matrix metalloproteinases in tumour invasion and metastasis. J Pathol 189:300–308

    Article  PubMed  CAS  Google Scholar 

  75. Garbett EA, Reed MW, Stephenson TJ, Brown NJ (2000) Proteolysis in human breast cancer. Mol Pathol 53:99–106

    Article  PubMed  CAS  Google Scholar 

  76. Parsons JT, Parsons SJ (1997) Src family protein tyrosine kinases: cooperating with growth factor and adhesion signaling pathways. Curr Opin Cell Biol 9:187–192

    Article  PubMed  CAS  Google Scholar 

  77. Yeatman TJ (2004) A renaissance for SRC. Nat Rev Cancer 4:470–480

    Article  PubMed  CAS  Google Scholar 

  78. Egan C, Pang A, Durda D, Cheng HC, Wang JH, Fujita DJ (1999) Activation of Src in human breast tumor cell lines: elevated levels of phosphotyrosine phosphatase activity that preferentially recognizes the Src carboxy terminal negative regulatory tyrosine 530. Oncogene 18:1227–1237

    Article  PubMed  CAS  Google Scholar 

  79. Jacobs C, Rubsamen H (1983) Expression of pp60c-src protein kinase in adult and fetal human tissue: high activities in some sarcomas and mammary carcinomas. Cancer Res 43:1696–1702

    PubMed  CAS  Google Scholar 

  80. Guy CT, Muthuswamy SK, Cardiff RD, Soriano P, Muller WJ (1984) Activation of the c-Src tyrosine kinase is required for the induction of mammary tumors in transgenic mice. Genes Dev 8:23–32

    Article  Google Scholar 

  81. Rosen N, Bolen JB, Schwartz AM, Cohen P, DeSeau V, Israel MA (1986) Analysis of pp60c-src protein kinase activity in human tumor cell lines and tissues. J Biol Chem 261:13754–13759

    PubMed  CAS  Google Scholar 

  82. Slack BE, Siniaia MS, Blusztajn JK (2006) Collagen type I selectively activates ectodomain shedding of the discoidin domain receptor 1: involvement of Src tyrosine kinase. J Cell Biochem 98:672–684

    Article  PubMed  CAS  Google Scholar 

  83. Sato H, Kita M, Seiki M (1993) v-Src activates the expression of 92-kDa type IV collagenase gene through the AP-1 site and the GT box homologous to retinoblastoma control elements. A mechanism regulating gene expression independent of that by inflammatory cytokines. J Biol Chem 268:23460–23468

    PubMed  CAS  Google Scholar 

  84. Hong IK, Jin YJ, Byun HJ, Jeoung DI, Kim YM, Lee H (2006) Homophilic interactions of Tetraspanin CD151 up-regulate motility and matrix metalloproteinase-9 expression of human melanoma cells through adhesion-dependent c-Jun activation signaling pathways. J Biol Chem 281:24279–24292

    Article  PubMed  CAS  Google Scholar 

  85. Vincenti MP, Coon CI, White LA, Barchowsky A, Brinckerhoff CE (1996) src-Related tyrosine kinases regulate transcriptional activation of the interstitial collagenase gene, MMP-1, in interleukin-1-stimulated synovial fibroblasts. Arthritis Rheum 39:574–582

    Article  PubMed  CAS  Google Scholar 

  86. Chen JM, Aimes RT, Ward GR, Youngleib GL, Quigley JP (1991) Isolation and characterization of a 70-kDa metalloprotease (gelatinase) that is elevated in Rous sarcoma virus-transformed chicken embryo fibroblasts. J Biol Chem 266:5113–5121

    PubMed  CAS  Google Scholar 

  87. Miyamori H, Hasegawa K, Kim KR, Sato H (2000) Expression of metastasis-associated mts1 gene is co-induced with membrane type-1 matrix metalloproteinase (MT1-MMP) during oncogenic transformation and tubular formation of Madin Darby canine kidney (MDCK) epithelial cells. Clin Exp Metastasis 18:51–56

    Article  PubMed  CAS  Google Scholar 

  88. Noritake H, Miyamori H, Goto C, Seiki M, Sato H (1999) Overexpression of tissue inhibitor of matrix metalloproteinases-1 (TIMP-1) in metastatic MDCK cells transformed by v-src. Clin Exp Metastasis 17:105–110

    Article  PubMed  CAS  Google Scholar 

  89. O’Brian C, Vogel VG, Singletary SE, Ward NE (1989) Elevated protein kinase C expression in human breast tumor biopsies relative to normal breast tissue. Cancer Res 49:3215–3217

    PubMed  Google Scholar 

  90. Takenaga K, Takahashi K (1986) Effects of 12-O-tetradecanoylphorbol-13-acetate on adhesiveness and lung-colonizing ability of Lewis lung carcinoma cells. Cancer Res 46:375–380

    PubMed  CAS  Google Scholar 

  91. Schwartz GK, Jiang J, Kelsen D, Albino AP (1993) Protein kinase C: a novel target for inhibiting gastric cancer cell invasion. J Natl Cancer Inst 85:402–407

    Article  PubMed  CAS  Google Scholar 

  92. Lane TA, Lamkin GE, Wancewicz E (1989) Modulation of endothelial cell expression of intercellular adhesion molecule 1 by protein kinase C activation. Biochem Biophys Res Commun 161:945–952

    Article  PubMed  CAS  Google Scholar 

  93. Rosse C, Linch M, Kermorgant S, Cameron AJ, Boeckeler K, Parker PJ (2010) PKC and the control of localized signal dynamics. Nat Rev Mol Cell Biol 11:103–112

    Article  PubMed  CAS  Google Scholar 

  94. Johnson MD, Torri JA, Lippman ME, Dickson RB (1999) Regulation of motility and protease expression in PKC-mediated induction of MCF-7 breast cancer cell invasiveness. Exp Cell Res 247:105–113

    Article  PubMed  CAS  Google Scholar 

  95. Aziz MH, Hafeez BB, Sand JM, Pierce DB, Aziz SW, Dreckschmidt NE, Verma AK (2010) Protein kinase Cvarepsilon mediates Stat3Ser727 phosphorylation, Stat3-regulated gene expression, and cell invasion in various human cancer cell lines through integration with MAPK cascade (RAF-1, MEK1/2, and ERK1/2). Oncogene 29:3100–3109

    Article  PubMed  CAS  Google Scholar 

  96. Ellerbroek SM, Hudson LG, Stack MS (1998) Proteinase requirements of epidermal growth factor-induced ovarian cancer cell invasion. Int J Cancer 78:331–337

    Article  PubMed  CAS  Google Scholar 

  97. Cox G, Jones JL, O’Byrne KJ (2000) Matrix metalloproteinase 9 and the epidermal growth factor signal pathway in operable non-small cell lung cancer. Clin Cancer Res 6:2349–2355

    PubMed  CAS  Google Scholar 

  98. Fischer OM, Hart S, Gschwind A, Ullrich A (2003) EGFR signal transactivation in cancer cells. Biochem Soc Trans 31:1203–1208

    Article  PubMed  CAS  Google Scholar 

  99. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, Ullrich A (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402:884–888

    PubMed  CAS  Google Scholar 

  100. Pai R, Soreghan B, Szabo IL, Pavelka M, Baatar D, Tarnawski AS (2002) Prostaglandin E2 transactivates EGF receptor: a novel mechanism for promoting colon cancer growth and gastrointestinal hypertrophy. Nat Med 8:289–293

    Article  PubMed  CAS  Google Scholar 

  101. Hyde CA, Missailidis S (2009) Inhibition of arachidonic acid metabolism and its implication on cell proliferation and tumour-angiogenesis. Int Immunopharmacol 9:701–715

    Article  PubMed  CAS  Google Scholar 

  102. Perez-Chacon G, Astudillo AM, Balgoma D, Balboa MA, Balsinde J (2009) Control of free arachidonic acid levels by phospholipases A2 and lysophospholipid acyltransferases. Biochim Biophys Acta 1791:1103–1113

    PubMed  CAS  Google Scholar 

  103. Brash AR (2001) Arachidonic acid as a bioactive molecule. J Clin Invest 107:1339–1345

    Article  PubMed  CAS  Google Scholar 

  104. Piomelli D (1993) Arachidonic acid in cell signaling. Curr Opin Cell Biol 5:274–280

    Article  PubMed  CAS  Google Scholar 

  105. Panini SR, Yang L, Rusinol AE, Sinensky MS, Bonventre JV, Leslie CC (2001) Arachidonate metabolism and the signaling pathway of induction of apoptosis by oxidized LDL/oxysterol. J Lipid Res 42:1678–1686

    PubMed  CAS  Google Scholar 

  106. Navarro-Tito N, Robledo T, Salazar EP (2008) Arachidonic acid promotes FAK activation and migration in MDA-MB-231 breast cancer cells. Exp Cell Res 314:3340–3355

    Article  PubMed  CAS  Google Scholar 

  107. Sumitani K, Kamijo R, Toyoshima T, Nakanishi Y, Takizawa K, Hatori M, Nagumo M (2001) Specific inhibition of cyclooxygenase-2 results in inhibition of proliferation of oral cancer cell lines via suppression of prostaglandin E2 production. J Oral Pathol Med 30:41–47

    Article  PubMed  CAS  Google Scholar 

  108. Kinugasa Y, Hatori M, Ito H, Kurihara Y, Ito D, Nagumo M (2004) Inhibition of cyclooxygenase-2 suppresses invasiveness of oral squamous cell carcinoma cell lines via down-regulation of matrix metalloproteinase-2 and CD44. Clin Exp Metastasis 21:737–745

    Article  PubMed  CAS  Google Scholar 

  109. Das S, Ongusaha PP, Yang YS, Park JM, Aaronson SA, Lee SW (2006) Discoidin domain receptor 1 receptor tyrosine kinase induces cyclooxygenase-2 and promotes chemoresistance through nuclear factor-kappaB pathway activation. Cancer Res 66:8123–8130

    Article  PubMed  CAS  Google Scholar 

  110. Singh NK, Quyen DV, Kundumani-Sridharan V, Brooks PC, Rao GN (2010) AP-1 (Fra-1/c-Jun)-mediated induction of expression of matrix metalloproteinase-2 is required for 15S-hydroxyeicosatetraenoic acid-induced angiogenesis. J Biol Chem 285:16830–16843

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to Nora Ruiz for her technical assistance and Victor Rosales-Garcia for his technical assistance at flow cytometry technique. This work was supported by a grant from CONACYT (83802). L.C.-S. was supported by a CONACYT predoctoral training grant and actually is supported by a Post-Doctoral fellowship from ICyTDF. A.S.-G. was supported by a Post-Doctoral fellowship from ICyTDF. M.G.-D. was supported by a Post-Doctoral grant from CONACYT (83802).

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  1. Departamento de Biologia Celular, Cinvestav-IPN, Av. IPN # 2508, San Pedro Zacatenco, 07360, Mexico, DF, Mexico

    Luis Castro-Sanchez, Adriana Soto-Guzman, Margarita Guaderrama-Diaz, Pedro Cortes-Reynosa & Eduardo Perez Salazar

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  1. Luis Castro-Sanchez
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  2. Adriana Soto-Guzman
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Correspondence to Eduardo Perez Salazar.

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Fig. S1

Native type IV collagen induces DDR1 tyrosine phosphorylation in MDA-MB-231 cells. MDA-MB-231 cells were treated without or with 7 μg/ml type IV collagen in solution (Col IV) for various times as indicated, and cells were lysed or integral membrane proteins were obtained. Panel a DDR1 protein expression was analyzed by Western-blotting of cell lysates with anti-DDR1 Ab. Panels b, c DDR1 tyrosine phosphorylation was analyzed by immunoprecipitation (IP) using anti-DDR1 Ab followed by Western-blotting with anti-P-Tyr Ab (PY20). The membranes were analyzed further by Western-blotting using anti-DDR1 Ab as loading control. The autoradiograms shown are representative of at least three independent experiments (TIFF 3390 kb)

Fig. S2

Denatured type IV collagen does not induce DDR1 tyrosine phosphorylation, whereas native type IV collagen induces invasiveness in MDA-MB-231 cells. Panel a MDA-MB-231 cells were treated without or with 7 μg/ml native type IV collagen or with 7 μg/ml denatured native type IV collagen for 10 and 25 h as indicated, and then integral membrane proteins were obtained. DDR1 tyrosine phosphorylation was analyzed by immunoprecipitation (IP) using anti-DDR1 Ab followed by Western-blotting with anti-Tyr(P) Ab (PY20). The membrane was analyzed further by Western-blotting using anti-DDR1 Ab as loading control. Denatured type IV collagen was prepared by heating the native type IV collagen solution at 90°C for 50 min. Panel b MDA-MB-231 cells held in suspension were treated for 2 h with 12 μM mitomycyn C, as indicated and then cells were plated on the top of matrigel and treated with 7 μg/ml native type IV collagen for various times, as indicated. Cell invasion was evaluated after incubation as described in “Material and methods” (TIFF 3087 kb)

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Castro-Sanchez, L., Soto-Guzman, A., Guaderrama-Diaz, M. et al. Role of DDR1 in the gelatinases secretion induced by native type IV collagen in MDA-MB-231 breast cancer cells. Clin Exp Metastasis 28, 463–477 (2011). https://doi.org/10.1007/s10585-011-9385-9

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  • DOI: https://doi.org/10.1007/s10585-011-9385-9

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