Skip to main content
Erschienen in: Angiogenesis 4/2013

01.10.2013 | Original Paper

Prostate specific membrane antigen produces pro-angiogenic laminin peptides downstream of matrix metalloprotease-2

verfasst von: Rebecca E. Conway, Kyle Joiner, Alex Patterson, David Bourgeois, Robert Rampp, Benjamin C. Hannah, Samantha McReynolds, John M. Elder, Hannah Gilfilen, Linda H. Shapiro

Erschienen in: Angiogenesis | Ausgabe 4/2013

Einloggen, um Zugang zu erhalten

Abstract

Prostate specific membrane antigen (PSMA) is a pro-angiogenic cell-surface protease that we previously demonstrated regulates blood vessel formation in a laminin and integrin β1-dependent manner. Here, we examine the principal mechanism of PSMA activation of integrin β1. We show that digesting laminin sequentially with recombinant matrix metalloprotease-2 (MMP-2) and PSMA generates small peptides that enhance endothelial cell adhesion and migration in vitro. We also provide evidence that these laminin peptides activate adhesion via integrin α6β1 and focal adhesion kinase. Using an in vivo Matrigel implant assay, we show that these MMP/PSMA-derived laminin peptides also increase angiogenesis in vivo. Together, our results reveal a novel mechanism of PSMA activation of angiogenesis by processing laminin downstream of MMP-2.
Literatur
1.
Zurück zum Zitat Sprenger CC, Plymate SR, Reed MJ (2010) Aging-related alterations in the extracellular matrix modulate the microenvironment and influence tumor progression. Int J Cancer J Int du Cancer 127(12):2739–2748. doi:10.1002/ijc.25615 CrossRef Sprenger CC, Plymate SR, Reed MJ (2010) Aging-related alterations in the extracellular matrix modulate the microenvironment and influence tumor progression. Int J Cancer J Int du Cancer 127(12):2739–2748. doi:10.​1002/​ijc.​25615 CrossRef
3.
Zurück zum Zitat Bremnes RM, Donnem T, Al-Saad S, Al-Shibli K, Andersen S, Sirera R, Camps C, Marinez I, Busund LT (2011) The role of tumor stroma in cancer progression and prognosis: emphasis on carcinoma-associated fibroblasts and non-small cell lung cancer. J Thorac Oncol 6(1):209–217. doi:10.1097/JTO.0b013e3181f8a1bd PubMedCrossRef Bremnes RM, Donnem T, Al-Saad S, Al-Shibli K, Andersen S, Sirera R, Camps C, Marinez I, Busund LT (2011) The role of tumor stroma in cancer progression and prognosis: emphasis on carcinoma-associated fibroblasts and non-small cell lung cancer. J Thorac Oncol 6(1):209–217. doi:10.​1097/​JTO.​0b013e3181f8a1bd​ PubMedCrossRef
4.
Zurück zum Zitat Schulz WA, Ingenwerth M, Djuidje CE, Hader C, Rahnenfuhrer J, Engers R (2010) Changes in cortical cytoskeletal and extracellular matrix gene expression in prostate cancer are related to oncogenic ERG deregulation. BMC cancer 10:505. doi:10.1186/1471-2407-10-505 PubMedCrossRef Schulz WA, Ingenwerth M, Djuidje CE, Hader C, Rahnenfuhrer J, Engers R (2010) Changes in cortical cytoskeletal and extracellular matrix gene expression in prostate cancer are related to oncogenic ERG deregulation. BMC cancer 10:505. doi:10.​1186/​1471-2407-10-505 PubMedCrossRef
5.
Zurück zum Zitat Humphries MJ, Olden K, Yamada KM (1986) A synthetic peptide from fibronectin inhibits experimental metastasis of murine melanoma cells. Science 233(4762):467–470PubMedCrossRef Humphries MJ, Olden K, Yamada KM (1986) A synthetic peptide from fibronectin inhibits experimental metastasis of murine melanoma cells. Science 233(4762):467–470PubMedCrossRef
6.
Zurück zum Zitat Ponce ML, Hibino S, Lebioda AM, Mochizuki M, Nomizu M, Kleinman HK (2003) Identification of a potent peptide antagonist to an active laminin-1 sequence that blocks angiogenesis and tumor growth. Cancer Res 63(16):5060–5064PubMed Ponce ML, Hibino S, Lebioda AM, Mochizuki M, Nomizu M, Kleinman HK (2003) Identification of a potent peptide antagonist to an active laminin-1 sequence that blocks angiogenesis and tumor growth. Cancer Res 63(16):5060–5064PubMed
8.
Zurück zum Zitat Maeshima Y, Colorado PC, Torre A, Holthaus KA, Grunkemeyer JA, Ericksen MB, Hopfer H, Xiao Y, Stillman IE, Kalluri R (2000) Distinct antitumor properties of a type IV collagen domain derived from basement membrane. J Biol Chem 275(28):21340–21348. doi:10.1074/jbc.M001956200 PubMedCrossRef Maeshima Y, Colorado PC, Torre A, Holthaus KA, Grunkemeyer JA, Ericksen MB, Hopfer H, Xiao Y, Stillman IE, Kalluri R (2000) Distinct antitumor properties of a type IV collagen domain derived from basement membrane. J Biol Chem 275(28):21340–21348. doi:10.​1074/​jbc.​M001956200 PubMedCrossRef
9.
Zurück zum Zitat O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88(2):277–285PubMedCrossRef O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88(2):277–285PubMedCrossRef
10.
Zurück zum Zitat O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Cao Y, Moses M, Lane WS, Sage EH, Folkman J (1994) Angiostatin: a circulating endothelial cell inhibitor that suppresses angiogenesis and tumor growth. Cold Spring Harb Symp Quant Biol 59:471–482PubMedCrossRef O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Cao Y, Moses M, Lane WS, Sage EH, Folkman J (1994) Angiostatin: a circulating endothelial cell inhibitor that suppresses angiogenesis and tumor growth. Cold Spring Harb Symp Quant Biol 59:471–482PubMedCrossRef
11.
Zurück zum Zitat Maeshima Y, Sudhakar A, Lively JC, Ueki K, Kharbanda S, Kahn CR, Sonenberg N, Hynes RO, Kalluri R (2002) Tumstatin, an endothelial cell-specific inhibitor of protein synthesis. Science 295(5552):140–143. doi:10.1126/science.1065298 PubMedCrossRef Maeshima Y, Sudhakar A, Lively JC, Ueki K, Kharbanda S, Kahn CR, Sonenberg N, Hynes RO, Kalluri R (2002) Tumstatin, an endothelial cell-specific inhibitor of protein synthesis. Science 295(5552):140–143. doi:10.​1126/​science.​1065298 PubMedCrossRef
12.
Zurück zum Zitat Kamphaus GD, Colorado PC, Panka DJ, Hopfer H, Ramchandran R, Torre A, Maeshima Y, Mier JW, Sukhatme VP, Kalluri R (2000) Canstatin, a novel matrix-derived inhibitor of angiogenesis and tumor growth. J Biol Chem 275(2):1209–1215PubMedCrossRef Kamphaus GD, Colorado PC, Panka DJ, Hopfer H, Ramchandran R, Torre A, Maeshima Y, Mier JW, Sukhatme VP, Kalluri R (2000) Canstatin, a novel matrix-derived inhibitor of angiogenesis and tumor growth. J Biol Chem 275(2):1209–1215PubMedCrossRef
13.
Zurück zum Zitat Felbor U, Mutsch Y, Grehn F, Muller CR, Kress W (1999) Ocular ochronosis in alkaptonuria patients carrying mutations in the homogentisate 1,2-dioxygenase gene. Br J Ophthalmol 83(6):680–683PubMedCrossRef Felbor U, Mutsch Y, Grehn F, Muller CR, Kress W (1999) Ocular ochronosis in alkaptonuria patients carrying mutations in the homogentisate 1,2-dioxygenase gene. Br J Ophthalmol 83(6):680–683PubMedCrossRef
14.
Zurück zum Zitat Xu J, Kim GM, Ahmed SH, Xu J, Yan P, Xu XM, Hsu CY (2001) Glucocorticoid receptor-mediated suppression of activator protein-1 activation and matrix metalloproteinase expression after spinal cord injury. J Neurosci Off J Soc Neurosci 21(1):92–97 Xu J, Kim GM, Ahmed SH, Xu J, Yan P, Xu XM, Hsu CY (2001) Glucocorticoid receptor-mediated suppression of activator protein-1 activation and matrix metalloproteinase expression after spinal cord injury. J Neurosci Off J Soc Neurosci 21(1):92–97
15.
Zurück zum Zitat Koshikawa N, Giannelli G, Cirulli V, Miyazaki K, Quaranta V (2000) Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 148(3):615–624PubMedCrossRef Koshikawa N, Giannelli G, Cirulli V, Miyazaki K, Quaranta V (2000) Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 148(3):615–624PubMedCrossRef
16.
Zurück zum Zitat Risau W, Lemmon V (1988) Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev Biol 125(2):441–450PubMedCrossRef Risau W, Lemmon V (1988) Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev Biol 125(2):441–450PubMedCrossRef
17.
Zurück zum Zitat Ljubimova JY, Fujita M, Khazenzon NM, Ljubimov AV, Black KL (2006) Changes in laminin isoforms associated with brain tumor invasion and angiogenesis. Front Biosci 11:81–88PubMedCrossRef Ljubimova JY, Fujita M, Khazenzon NM, Ljubimov AV, Black KL (2006) Changes in laminin isoforms associated with brain tumor invasion and angiogenesis. Front Biosci 11:81–88PubMedCrossRef
18.
Zurück zum Zitat Kibbey MC, Grant DS, Kleinman HK (1992) Role of the SIKVAV site of laminin in promotion of angiogenesis and tumor growth: an in vivo Matrigel model. J Natl Cancer Inst 84(21):1633–1638PubMedCrossRef Kibbey MC, Grant DS, Kleinman HK (1992) Role of the SIKVAV site of laminin in promotion of angiogenesis and tumor growth: an in vivo Matrigel model. J Natl Cancer Inst 84(21):1633–1638PubMedCrossRef
19.
Zurück zum Zitat Malinda KM, Nomizu M, Chung M, Delgado M, Kuratomi Y, Yamada Y, Kleinman HK, Ponce ML (1999) Identification of laminin α1 and β1 chain peptides active for endothelial cell adhesion, tube formation, and aortic sprouting. FASEB J 13(1):53–62PubMed Malinda KM, Nomizu M, Chung M, Delgado M, Kuratomi Y, Yamada Y, Kleinman HK, Ponce ML (1999) Identification of laminin α1 and β1 chain peptides active for endothelial cell adhesion, tube formation, and aortic sprouting. FASEB J 13(1):53–62PubMed
21.
Zurück zum Zitat Nomizu M, Weeks BS, Weston CA, Kim WH, Kleinman HK, Yamada Y (1995) Structure-activity study of a laminin α1 chain active peptide segment Ile-Lys-Val-Ala-Val (IKVAV). FEBS Lett 365(2–3):227–231PubMedCrossRef Nomizu M, Weeks BS, Weston CA, Kim WH, Kleinman HK, Yamada Y (1995) Structure-activity study of a laminin α1 chain active peptide segment Ile-Lys-Val-Ala-Val (IKVAV). FEBS Lett 365(2–3):227–231PubMedCrossRef
22.
Zurück zum Zitat Aumailley M, Timpl R, Risau W (1991) Differences in laminin fragment interactions of normal and transformed endothelial cells. Exp Cell Res 196(2):177–183PubMedCrossRef Aumailley M, Timpl R, Risau W (1991) Differences in laminin fragment interactions of normal and transformed endothelial cells. Exp Cell Res 196(2):177–183PubMedCrossRef
23.
Zurück zum Zitat Wu ZS, Wu Q, Yang JH, Wang HQ, Ding XD, Yang F, Xu XC (2008) Prognostic significance of MMP-9 and TIMP-1 serum and tissue expression in breast cancer. Int J Cancer J Int du Cancer 122(9):2050–2056. doi:10.1002/ijc.23337 CrossRef Wu ZS, Wu Q, Yang JH, Wang HQ, Ding XD, Yang F, Xu XC (2008) Prognostic significance of MMP-9 and TIMP-1 serum and tissue expression in breast cancer. Int J Cancer J Int du Cancer 122(9):2050–2056. doi:10.​1002/​ijc.​23337 CrossRef
24.
25.
Zurück zum Zitat Poola I, DeWitty RL, Marshalleck JJ, Bhatnagar R, Abraham J, Leffall LD (2005) Identification of MMP-1 as a putative breast cancer predictive marker by global gene expression analysis. Nat Med 11(5):481–483. doi:10.1038/nm1243 PubMedCrossRef Poola I, DeWitty RL, Marshalleck JJ, Bhatnagar R, Abraham J, Leffall LD (2005) Identification of MMP-1 as a putative breast cancer predictive marker by global gene expression analysis. Nat Med 11(5):481–483. doi:10.​1038/​nm1243 PubMedCrossRef
26.
Zurück zum Zitat Koc M, Ediger D, Budak F, Karadag M, Oral HB, Uzaslan E, Ege E, Gozu RO (2006) Matrix metalloproteinase-9 (MMP-9) elevated in serum but not in bronchial lavage fluid in patients with lung cancer. Tumori 92(2):149–154PubMed Koc M, Ediger D, Budak F, Karadag M, Oral HB, Uzaslan E, Ege E, Gozu RO (2006) Matrix metalloproteinase-9 (MMP-9) elevated in serum but not in bronchial lavage fluid in patients with lung cancer. Tumori 92(2):149–154PubMed
27.
Zurück zum Zitat Morgia G, Falsaperla M, Malaponte G, Madonia M, Indelicato M, Travali S, Mazzarino MC (2005) Matrix metalloproteinases as diagnostic (MMP-13) and prognostic (MMP-2, MMP-9) markers of prostate cancer. Urol Res 33(1):44–50. doi:10.1007/s00240-004-0440-8 PubMedCrossRef Morgia G, Falsaperla M, Malaponte G, Madonia M, Indelicato M, Travali S, Mazzarino MC (2005) Matrix metalloproteinases as diagnostic (MMP-13) and prognostic (MMP-2, MMP-9) markers of prostate cancer. Urol Res 33(1):44–50. doi:10.​1007/​s00240-004-0440-8 PubMedCrossRef
28.
Zurück zum Zitat Montesano R, Mouron P, Orci L (1985) Vascular outgrowths from tissue explants embedded in fibrin or collagen gels: a simple in vitro model of angiogenesis. Cell Biol Int Rep 9(10):869–875PubMedCrossRef Montesano R, Mouron P, Orci L (1985) Vascular outgrowths from tissue explants embedded in fibrin or collagen gels: a simple in vitro model of angiogenesis. Cell Biol Int Rep 9(10):869–875PubMedCrossRef
30.
Zurück zum Zitat Folkman J, Klagsbrun M, Sasse J, Wadzinski M, Ingber D, Vlodavsky I (1988) A heparin-binding angiogenic protein-basic fibroblast growth factor is stored within basement membrane. Am J Pathol 130(2):393–400PubMed Folkman J, Klagsbrun M, Sasse J, Wadzinski M, Ingber D, Vlodavsky I (1988) A heparin-binding angiogenic protein-basic fibroblast growth factor is stored within basement membrane. Am J Pathol 130(2):393–400PubMed
31.
Zurück zum Zitat O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH, Folkman J (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79(2):315–328PubMedCrossRef O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH, Folkman J (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79(2):315–328PubMedCrossRef
32.
Zurück zum Zitat Lane TF, Iruela-Arispe ML, Johnson RS, Sage EH (1994) SPARC is a source of copper-binding peptides that stimulate angiogenesis. J Cell Biol 125(4):929–943PubMedCrossRef Lane TF, Iruela-Arispe ML, Johnson RS, Sage EH (1994) SPARC is a source of copper-binding peptides that stimulate angiogenesis. J Cell Biol 125(4):929–943PubMedCrossRef
34.
Zurück zum Zitat McDaniel SM, Rumer KK, Biroc SL, Metz RP, Singh M, Porter W, Schedin P (2006) Remodeling of the mammary microenvironment after lactation promotes breast tumor cell metastasis. Am J Pathology 168(2):608–620. doi:10.2353/ajpath.2006.050677 CrossRef McDaniel SM, Rumer KK, Biroc SL, Metz RP, Singh M, Porter W, Schedin P (2006) Remodeling of the mammary microenvironment after lactation promotes breast tumor cell metastasis. Am J Pathology 168(2):608–620. doi:10.​2353/​ajpath.​2006.​050677 CrossRef
35.
36.
Zurück zum Zitat Bhagwat SV, Lahdenranta J, Giordano R, Arap W, Pasqualini R, Shapiro LH (2001) CD13/APN is activated by angiogenic signals and is essential for capillary tube formation. Blood 97(3):652–659PubMedCrossRef Bhagwat SV, Lahdenranta J, Giordano R, Arap W, Pasqualini R, Shapiro LH (2001) CD13/APN is activated by angiogenic signals and is essential for capillary tube formation. Blood 97(3):652–659PubMedCrossRef
37.
Zurück zum Zitat Chen J, Zhang ZG, Li Y, Wang Y, Wang L, Jiang H, Zhang C, Lu M, Katakowski M, Feldkamp CS, Chopp M (2003) Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 53(6):743–751. doi:10.1002/ana.10555 PubMedCrossRef Chen J, Zhang ZG, Li Y, Wang Y, Wang L, Jiang H, Zhang C, Lu M, Katakowski M, Feldkamp CS, Chopp M (2003) Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 53(6):743–751. doi:10.​1002/​ana.​10555 PubMedCrossRef
38.
Zurück zum Zitat Marchio S, Lahdenranta J, Schlingemann RO, Valdembri D, Wesseling P, Arap MA, Hajitou A, Ozawa MG, Trepel M, Giordano RJ, Nanus DM, Dijkman HB, Oosterwijk E, Sidman RL, Cooper MD, Bussolino F, Pasqualini R, Arap W (2004) Aminopeptidase A is a functional target in angiogenic blood vessels. Cancer Cell 5(2):151–162PubMedCrossRef Marchio S, Lahdenranta J, Schlingemann RO, Valdembri D, Wesseling P, Arap MA, Hajitou A, Ozawa MG, Trepel M, Giordano RJ, Nanus DM, Dijkman HB, Oosterwijk E, Sidman RL, Cooper MD, Bussolino F, Pasqualini R, Arap W (2004) Aminopeptidase A is a functional target in angiogenic blood vessels. Cancer Cell 5(2):151–162PubMedCrossRef
39.
Zurück zum Zitat Conway RE, Petrovic N, Li Z, Heston W, Wu D, Shapiro LH (2006) Prostate-specific membrane antigen regulates angiogenesis by modulating integrin signal transduction. Mol Cell Biol 26(14):5310–5324. doi:10.1128/MCB.00084-06 PubMedCrossRef Conway RE, Petrovic N, Li Z, Heston W, Wu D, Shapiro LH (2006) Prostate-specific membrane antigen regulates angiogenesis by modulating integrin signal transduction. Mol Cell Biol 26(14):5310–5324. doi:10.​1128/​MCB.​00084-06 PubMedCrossRef
40.
Zurück zum Zitat Horoszewicz JS, Kawinski E, Murphy GP (1987) Monoclonal antibodies to a new antigenic marker in epithelial prostatic cells and serum of prostatic cancer patients. Anticancer Res 7(5B):927–935PubMed Horoszewicz JS, Kawinski E, Murphy GP (1987) Monoclonal antibodies to a new antigenic marker in epithelial prostatic cells and serum of prostatic cancer patients. Anticancer Res 7(5B):927–935PubMed
41.
Zurück zum Zitat Israeli RS, Powell CT, Fair WR, Heston WD (1993) Molecular cloning of a complementary DNA encoding a prostate-specific membrane antigen. Cancer Res 53(2):227–230PubMed Israeli RS, Powell CT, Fair WR, Heston WD (1993) Molecular cloning of a complementary DNA encoding a prostate-specific membrane antigen. Cancer Res 53(2):227–230PubMed
42.
Zurück zum Zitat Israeli RS, Miller WH Jr, Su SL, Samadi DS, Powell CT, Heston WD, Wise GJ, Fair WR (1995) Sensitive detection of prostatic hematogenous tumor cell dissemination using prostate specific antigen and prostate specific membrane-derived primers in the polymerase chain reaction. J Urol 153(3 Pt 1):573–577PubMed Israeli RS, Miller WH Jr, Su SL, Samadi DS, Powell CT, Heston WD, Wise GJ, Fair WR (1995) Sensitive detection of prostatic hematogenous tumor cell dissemination using prostate specific antigen and prostate specific membrane-derived primers in the polymerase chain reaction. J Urol 153(3 Pt 1):573–577PubMed
43.
Zurück zum Zitat Drachenberg DE, Elgamal AA, Rowbotham R, Peterson M, Murphy GP (1999) Circulating levels of interleukin-6 in patients with hormone refractory prostate cancer. Prostate 41(2):127–133PubMedCrossRef Drachenberg DE, Elgamal AA, Rowbotham R, Peterson M, Murphy GP (1999) Circulating levels of interleukin-6 in patients with hormone refractory prostate cancer. Prostate 41(2):127–133PubMedCrossRef
44.
Zurück zum Zitat Liu H, Moy P, Kim S, Xia Y, Rajasekaran A, Navarro V, Knudsen B, Bander NH (1997) Monoclonal antibodies to the extracellular domain of prostate-specific membrane antigen also react with tumor vascular endothelium. Cancer Res 57(17):3629–3634PubMed Liu H, Moy P, Kim S, Xia Y, Rajasekaran A, Navarro V, Knudsen B, Bander NH (1997) Monoclonal antibodies to the extracellular domain of prostate-specific membrane antigen also react with tumor vascular endothelium. Cancer Res 57(17):3629–3634PubMed
45.
Zurück zum Zitat Silver DA, Pellicer I, Fair WR, Heston WD, Cordon-Cardo C (1997) Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res Off J Am Assoc Cancer Res 3(1):81–85 Silver DA, Pellicer I, Fair WR, Heston WD, Cordon-Cardo C (1997) Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res Off J Am Assoc Cancer Res 3(1):81–85
46.
Zurück zum Zitat Chang SS, Heston WD (2002) The clinical role of prostate-specific membrane antigen (PSMA). Urol Oncol 7(1):7–12PubMedCrossRef Chang SS, Heston WD (2002) The clinical role of prostate-specific membrane antigen (PSMA). Urol Oncol 7(1):7–12PubMedCrossRef
47.
Zurück zum Zitat Carter RE, Feldman AR, Coyle JT (1996) Prostate-specific membrane antigen is a hydrolase with substrate and pharmacologic characteristics of a neuropeptidase. Proc Natl Acad Sci USA 93(2):749–753PubMedCrossRef Carter RE, Feldman AR, Coyle JT (1996) Prostate-specific membrane antigen is a hydrolase with substrate and pharmacologic characteristics of a neuropeptidase. Proc Natl Acad Sci USA 93(2):749–753PubMedCrossRef
48.
Zurück zum Zitat Tiffany CW, Lapidus RG, Merion A, Calvin DC, Slusher BS (1999) Characterization of the enzymatic activity of PSM: comparison with brain NAALADase. Prostate 39(1):28–35PubMedCrossRef Tiffany CW, Lapidus RG, Merion A, Calvin DC, Slusher BS (1999) Characterization of the enzymatic activity of PSM: comparison with brain NAALADase. Prostate 39(1):28–35PubMedCrossRef
49.
Zurück zum Zitat Pinto JT, Suffoletto BP, Berzin TM, Qiao CH, Lin S, Tong WP, May F, Mukherjee B, Heston WD (1996) Prostate-specific membrane antigen: a novel folate hydrolase in human prostatic carcinoma cells. Clin Cancer Res Off J Am Assoc Cancer Res 2(9):1445–1451 Pinto JT, Suffoletto BP, Berzin TM, Qiao CH, Lin S, Tong WP, May F, Mukherjee B, Heston WD (1996) Prostate-specific membrane antigen: a novel folate hydrolase in human prostatic carcinoma cells. Clin Cancer Res Off J Am Assoc Cancer Res 2(9):1445–1451
50.
51.
Zurück zum Zitat Fujita M, Khazenzon NM, Bose S, Sekiguchi K, Sasaki T, Carter WG, Ljubimov AV, Black KL, Ljubimova JY (2005) Overexpression of β1-chain-containing laminins in capillary basement membranes of human breast cancer and its metastases. Breast Cancer Res BCR 7(4):R411–R421. doi:10.1186/bcr1011 CrossRef Fujita M, Khazenzon NM, Bose S, Sekiguchi K, Sasaki T, Carter WG, Ljubimov AV, Black KL, Ljubimova JY (2005) Overexpression of β1-chain-containing laminins in capillary basement membranes of human breast cancer and its metastases. Breast Cancer Res BCR 7(4):R411–R421. doi:10.​1186/​bcr1011 CrossRef
53.
Zurück zum Zitat Mesters JR, Barinka C, Li W, Tsukamoto T, Majer P, Slusher BS, Konvalinka J, Hilgenfeld R (2006) Structure of glutamate carboxypeptidase II, a drug target in neuronal damage and prostate cancer. EMBO J 25(6):1375–1384. doi:10.1038/sj.emboj.7600969 PubMedCrossRef Mesters JR, Barinka C, Li W, Tsukamoto T, Majer P, Slusher BS, Konvalinka J, Hilgenfeld R (2006) Structure of glutamate carboxypeptidase II, a drug target in neuronal damage and prostate cancer. EMBO J 25(6):1375–1384. doi:10.​1038/​sj.​emboj.​7600969 PubMedCrossRef
55.
Zurück zum Zitat Mydel P, Shipley JM, Adair-Kirk TL, Kelley DG, Broekelmann TJ, Mecham RP, Senior RM (2008) Neutrophil elastase cleaves laminin-332 (laminin-5) generating peptides that are chemotactic for neutrophils. J Biol Chem 283(15):9513–9522. doi:10.1074/jbc.M706239200 PubMedCrossRef Mydel P, Shipley JM, Adair-Kirk TL, Kelley DG, Broekelmann TJ, Mecham RP, Senior RM (2008) Neutrophil elastase cleaves laminin-332 (laminin-5) generating peptides that are chemotactic for neutrophils. J Biol Chem 283(15):9513–9522. doi:10.​1074/​jbc.​M706239200 PubMedCrossRef
56.
Zurück zum Zitat Udayakumar TS, Chen ML, Bair EL, Von Bredow DC, Cress AE, Nagle RB, Bowden GT (2003) Membrane type-1-matrix metalloproteinase expressed by prostate carcinoma cells cleaves human laminin-5 β3 chain and induces cell migration. Cancer Res 63(9):2292–2299PubMed Udayakumar TS, Chen ML, Bair EL, Von Bredow DC, Cress AE, Nagle RB, Bowden GT (2003) Membrane type-1-matrix metalloproteinase expressed by prostate carcinoma cells cleaves human laminin-5 β3 chain and induces cell migration. Cancer Res 63(9):2292–2299PubMed
57.
Zurück zum Zitat Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y (1997) Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 272(4):2446–2451PubMedCrossRef Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y (1997) Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 272(4):2446–2451PubMedCrossRef
58.
Zurück zum Zitat Littlepage LE, Sternlicht MD, Rougier N, Phillips J, Gallo E, Yu Y, Williams K, Brenot A, Gordon JI, Werb Z (2010) Matrix metalloproteinases contribute distinct roles in neuroendocrine prostate carcinogenesis, metastasis, and angiogenesis progression. Cancer Res 70(6):2224–2234. doi:10.1158/0008-5472.CAN-09-3515 PubMedCrossRef Littlepage LE, Sternlicht MD, Rougier N, Phillips J, Gallo E, Yu Y, Williams K, Brenot A, Gordon JI, Werb Z (2010) Matrix metalloproteinases contribute distinct roles in neuroendocrine prostate carcinogenesis, metastasis, and angiogenesis progression. Cancer Res 70(6):2224–2234. doi:10.​1158/​0008-5472.​CAN-09-3515 PubMedCrossRef
59.
Zurück zum Zitat Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V (1997) Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277(5323):225–228PubMedCrossRef Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V (1997) Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277(5323):225–228PubMedCrossRef
60.
Zurück zum Zitat Giannelli G, Bergamini C, Fransvea E, Marinosci F, Quaranta V, Antonaci S (2001) Human hepatocellular carcinoma (HCC) cells require both α3β1 integrin and matrix metalloproteinases activity for migration and invasion. Lab Invest J Tech Methods Pathol 81(4):613–627CrossRef Giannelli G, Bergamini C, Fransvea E, Marinosci F, Quaranta V, Antonaci S (2001) Human hepatocellular carcinoma (HCC) cells require both α3β1 integrin and matrix metalloproteinases activity for migration and invasion. Lab Invest J Tech Methods Pathol 81(4):613–627CrossRef
61.
Zurück zum Zitat Gu J, Nishiuchi R, Sekiguchi K (2002) Matrix metalloproteinase-2 is involved in A549 cell migration on laminin-10/11. Biochem Biophys Res Commun 296(1):73–77PubMedCrossRef Gu J, Nishiuchi R, Sekiguchi K (2002) Matrix metalloproteinase-2 is involved in A549 cell migration on laminin-10/11. Biochem Biophys Res Commun 296(1):73–77PubMedCrossRef
62.
Zurück zum Zitat Heath TG, Giordani AB (1993) Reversed-phase capillary high-performance liquid chromatography with on-line UV, fluorescence and electrospray ionization mass spectrometric detection in the analysis of peptides and proteins. J Chromatogr 638(1):9–19PubMedCrossRef Heath TG, Giordani AB (1993) Reversed-phase capillary high-performance liquid chromatography with on-line UV, fluorescence and electrospray ionization mass spectrometric detection in the analysis of peptides and proteins. J Chromatogr 638(1):9–19PubMedCrossRef
63.
Zurück zum Zitat Igarashi Y, Heureux E, Doctor KS, Talwar P, Gramatikova S, Gramatikoff K, Zhang Y, Blinov M, Ibragimova SS, Boyd S, Ratnikov B, Cieplak P, Godzik A, Smith JW, Osterman AL, Eroshkin AM (2009) PMAP: databases for analyzing proteolytic events and pathways. Nucleic Acids Res 37(Database issue):D611–D618. doi:10.1093/nar/gkn683 PubMedCrossRef Igarashi Y, Heureux E, Doctor KS, Talwar P, Gramatikova S, Gramatikoff K, Zhang Y, Blinov M, Ibragimova SS, Boyd S, Ratnikov B, Cieplak P, Godzik A, Smith JW, Osterman AL, Eroshkin AM (2009) PMAP: databases for analyzing proteolytic events and pathways. Nucleic Acids Res 37(Database issue):D611–D618. doi:10.​1093/​nar/​gkn683 PubMedCrossRef
65.
Zurück zum Zitat Makino M, Okazaki I, Kasai S, Nishi N, Bougaeva M, Weeks BS, Otaka A, Nielsen PK, Yamada Y, Nomizu M (2002) Identification of cell binding sites in the laminin α5-chain G domain. Exp Cell Res 277(1):95–106. doi:10.1006/excr.2002.5540 PubMedCrossRef Makino M, Okazaki I, Kasai S, Nishi N, Bougaeva M, Weeks BS, Otaka A, Nielsen PK, Yamada Y, Nomizu M (2002) Identification of cell binding sites in the laminin α5-chain G domain. Exp Cell Res 277(1):95–106. doi:10.​1006/​excr.​2002.​5540 PubMedCrossRef
66.
Zurück zum Zitat Baker AH, Wilkinson GW, Hembry RM, Murphy G, Newby AC (1996) Development of recombinant adenoviruses that drive high level expression of the human metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 and -2 genes: characterization of their infection into rabbit smooth muscle cells and human MCF-7 adenocarcinoma cells. Matrix Biol J Int Soc Matrix Biol 15(6):383–395CrossRef Baker AH, Wilkinson GW, Hembry RM, Murphy G, Newby AC (1996) Development of recombinant adenoviruses that drive high level expression of the human metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 and -2 genes: characterization of their infection into rabbit smooth muscle cells and human MCF-7 adenocarcinoma cells. Matrix Biol J Int Soc Matrix Biol 15(6):383–395CrossRef
68.
Zurück zum Zitat Carter WG, Wayner EA, Bouchard TS, Kaur P (1990) The role of integrins α2β1 and α3β1 in cell-cell and cell-substrate adhesion of human epidermal cells. J Cell Biol 110(4):1387–1404PubMedCrossRef Carter WG, Wayner EA, Bouchard TS, Kaur P (1990) The role of integrins α2β1 and α3β1 in cell-cell and cell-substrate adhesion of human epidermal cells. J Cell Biol 110(4):1387–1404PubMedCrossRef
69.
Zurück zum Zitat Kramer RH (1994) Characterization of laminin-binding integrins. Methods Enzymol 245:129–147PubMedCrossRef Kramer RH (1994) Characterization of laminin-binding integrins. Methods Enzymol 245:129–147PubMedCrossRef
70.
Zurück zum Zitat Lee TH, Seng S, Li H, Kennel SJ, Avraham HK, Avraham S (2006) Integrin regulation by vascular endothelial growth factor in human brain microvascular endothelial cells: role of α6β1 integrin in angiogenesis. J Biol Chem 281(52):40450–40460. doi:10.1074/jbc.M607525200 PubMedCrossRef Lee TH, Seng S, Li H, Kennel SJ, Avraham HK, Avraham S (2006) Integrin regulation by vascular endothelial growth factor in human brain microvascular endothelial cells: role of α6β1 integrin in angiogenesis. J Biol Chem 281(52):40450–40460. doi:10.​1074/​jbc.​M607525200 PubMedCrossRef
71.
Zurück zum Zitat Witkowski CM, Rabinovitz I, Nagle RB, Affinito KS, Cress AE (1993) Characterization of integrin subunits, cellular adhesion and tumorgenicity of four human prostate cell lines. J Cancer Res Clin Oncol 119(11):637–644PubMedCrossRef Witkowski CM, Rabinovitz I, Nagle RB, Affinito KS, Cress AE (1993) Characterization of integrin subunits, cellular adhesion and tumorgenicity of four human prostate cell lines. J Cancer Res Clin Oncol 119(11):637–644PubMedCrossRef
72.
Zurück zum Zitat da Silva RG, Tavora B, Robinson SD, Reynolds LE, Szekeres C, Lamar J, Batista S, Kostourou V, Germain MA, Reynolds AR, Jones DT, Watson AR, Jones JL, Harris A, Hart IR, Iruela-Arispe ML, Dipersio CM, Kreidberg JA, Hodivala-Dilke KM (2010) Endothelial α3β1-integrin represses pathological angiogenesis and sustains endothelial-VEGF. Am J Pathol 177(3):1534–1548. doi:10.2353/ajpath.2010.100043 PubMedCrossRef da Silva RG, Tavora B, Robinson SD, Reynolds LE, Szekeres C, Lamar J, Batista S, Kostourou V, Germain MA, Reynolds AR, Jones DT, Watson AR, Jones JL, Harris A, Hart IR, Iruela-Arispe ML, Dipersio CM, Kreidberg JA, Hodivala-Dilke KM (2010) Endothelial α3β1-integrin represses pathological angiogenesis and sustains endothelial-VEGF. Am J Pathol 177(3):1534–1548. doi:10.​2353/​ajpath.​2010.​100043 PubMedCrossRef
73.
Zurück zum Zitat Ido H, Harada K, Futaki S, Hayashi Y, Nishiuchi R, Natsuka Y, Li S, Wada Y, Combs AC, Ervasti JM, Sekiguchi K (2004) Molecular dissection of the alpha-dystroglycan- and integrin-binding sites within the globular domain of human laminin-10. J Biol Chem 279(12):10946–10954. doi:10.1074/jbc.M313626200 PubMedCrossRef Ido H, Harada K, Futaki S, Hayashi Y, Nishiuchi R, Natsuka Y, Li S, Wada Y, Combs AC, Ervasti JM, Sekiguchi K (2004) Molecular dissection of the alpha-dystroglycan- and integrin-binding sites within the globular domain of human laminin-10. J Biol Chem 279(12):10946–10954. doi:10.​1074/​jbc.​M313626200 PubMedCrossRef
74.
Zurück zum Zitat Kunneken K, Pohlentz G, Schmidt-Hederich A, Odenthal U, Smyth N, Peter-Katalinic J, Bruckner P, Eble JA (2004) Recombinant human laminin-5 domains. Effects of heterotrimerization, proteolytic processing, and N-glycosylation on α3β1 integrin binding. J Biol Chem 279(7):5184–5193. doi:10.1074/jbc.M310424200 PubMedCrossRef Kunneken K, Pohlentz G, Schmidt-Hederich A, Odenthal U, Smyth N, Peter-Katalinic J, Bruckner P, Eble JA (2004) Recombinant human laminin-5 domains. Effects of heterotrimerization, proteolytic processing, and N-glycosylation on α3β1 integrin binding. J Biol Chem 279(7):5184–5193. doi:10.​1074/​jbc.​M310424200 PubMedCrossRef
75.
Zurück zum Zitat Ido H, Nakamura A, Kobayashi R, Ito S, Li S, Futaki S, Sekiguchi K (2007) The requirement of the glutamic acid residue at the third position from the carboxyl termini of the laminin gamma chains in integrin binding by laminins. J Biol Chem 282(15):11144–11154. doi:10.1074/jbc.M609402200 PubMedCrossRef Ido H, Nakamura A, Kobayashi R, Ito S, Li S, Futaki S, Sekiguchi K (2007) The requirement of the glutamic acid residue at the third position from the carboxyl termini of the laminin gamma chains in integrin binding by laminins. J Biol Chem 282(15):11144–11154. doi:10.​1074/​jbc.​M609402200 PubMedCrossRef
76.
Zurück zum Zitat Taniguchi Y, Ido H, Sanzen N, Hayashi M, Sato-Nishiuchi R, Futaki S, Sekiguchi K (2009) The C-terminal region of laminin beta chains modulates the integrin binding affinities of laminins. J Biol Chem 284(12):7820–7831. doi:10.1074/jbc.M809332200 PubMedCrossRef Taniguchi Y, Ido H, Sanzen N, Hayashi M, Sato-Nishiuchi R, Futaki S, Sekiguchi K (2009) The C-terminal region of laminin beta chains modulates the integrin binding affinities of laminins. J Biol Chem 284(12):7820–7831. doi:10.​1074/​jbc.​M809332200 PubMedCrossRef
77.
Zurück zum Zitat Vorup-Jensen T, Petersen SV, Hansen AG, Poulsen K, Schwaeble W, Sim RB, Reid KB, Davis SJ, Thiel S, Jensenius JC (2000) Distinct pathways of mannan-binding lectin (MBL)- and C1-complex autoactivation revealed by reconstitution of MBL with recombinant MBL-associated serine protease-2. J Immunol 165(4):2093–2100PubMed Vorup-Jensen T, Petersen SV, Hansen AG, Poulsen K, Schwaeble W, Sim RB, Reid KB, Davis SJ, Thiel S, Jensenius JC (2000) Distinct pathways of mannan-binding lectin (MBL)- and C1-complex autoactivation revealed by reconstitution of MBL with recombinant MBL-associated serine protease-2. J Immunol 165(4):2093–2100PubMed
78.
Zurück zum Zitat Wickstrom SA, Alitalo K, Keski-Oja J (2004) An endostatin-derived peptide interacts with integrins and regulates actin cytoskeleton and migration of endothelial cells. J Biol Chem 279(19):20178–20185. doi:10.1074/jbc.M312921200 PubMedCrossRef Wickstrom SA, Alitalo K, Keski-Oja J (2004) An endostatin-derived peptide interacts with integrins and regulates actin cytoskeleton and migration of endothelial cells. J Biol Chem 279(19):20178–20185. doi:10.​1074/​jbc.​M312921200 PubMedCrossRef
79.
81.
Zurück zum Zitat Shimaoka T, Nakayama T, Fukumoto N, Kume N, Takahashi S, Yamaguchi J, Minami M, Hayashida K, Kita T, Ohsumi J, Yoshie O, Yonehara S (2004) Cell surface-anchored SR-PSOX/CXC chemokine ligand 16 mediates firm adhesion of CXC chemokine receptor 6-expressing cells. J Leukoc Biol 75(2):267–274. doi:10.1189/jlb.1003465 PubMedCrossRef Shimaoka T, Nakayama T, Fukumoto N, Kume N, Takahashi S, Yamaguchi J, Minami M, Hayashida K, Kita T, Ohsumi J, Yoshie O, Yonehara S (2004) Cell surface-anchored SR-PSOX/CXC chemokine ligand 16 mediates firm adhesion of CXC chemokine receptor 6-expressing cells. J Leukoc Biol 75(2):267–274. doi:10.​1189/​jlb.​1003465 PubMedCrossRef
82.
Zurück zum Zitat Weathington NM, van Houwelingen AH, Noerager BD, Jackson PL, Kraneveld AD, Galin FS, Folkerts G, Nijkamp FP, Blalock JE (2006) A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat Med 12(3):317–323. doi:10.1038/nm1361 PubMedCrossRef Weathington NM, van Houwelingen AH, Noerager BD, Jackson PL, Kraneveld AD, Galin FS, Folkerts G, Nijkamp FP, Blalock JE (2006) A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat Med 12(3):317–323. doi:10.​1038/​nm1361 PubMedCrossRef
83.
Zurück zum Zitat Gaggar A, Jackson PL, Noerager BD, O’Reilly PJ, McQuaid DB, Rowe SM, Clancy JP, Blalock JE (2008) A novel proteolytic cascade generates an extracellular matrix-derived chemoattractant in chronic neutrophilic inflammation. J Immunol 180(8):5662–5669PubMed Gaggar A, Jackson PL, Noerager BD, O’Reilly PJ, McQuaid DB, Rowe SM, Clancy JP, Blalock JE (2008) A novel proteolytic cascade generates an extracellular matrix-derived chemoattractant in chronic neutrophilic inflammation. J Immunol 180(8):5662–5669PubMed
Metadaten
Titel
Prostate specific membrane antigen produces pro-angiogenic laminin peptides downstream of matrix metalloprotease-2
verfasst von
Rebecca E. Conway
Kyle Joiner
Alex Patterson
David Bourgeois
Robert Rampp
Benjamin C. Hannah
Samantha McReynolds
John M. Elder
Hannah Gilfilen
Linda H. Shapiro
Publikationsdatum
01.10.2013
Verlag
Springer Netherlands
Erschienen in
Angiogenesis / Ausgabe 4/2013
Print ISSN: 0969-6970
Elektronische ISSN: 1573-7209
DOI
https://doi.org/10.1007/s10456-013-9360-y

Weitere Artikel der Ausgabe 4/2013

Angiogenesis 4/2013 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Echinokokkose medikamentös behandeln oder operieren?

06.05.2024 DCK 2024 Kongressbericht

Die Therapie von Echinokokkosen sollte immer in spezialisierten Zentren erfolgen. Eine symptomlose Echinokokkose kann – egal ob von Hunde- oder Fuchsbandwurm ausgelöst – konservativ erfolgen. Wenn eine Op. nötig ist, kann es sinnvoll sein, vorher Zysten zu leeren und zu desinfizieren. 

Umsetzung der POMGAT-Leitlinie läuft

03.05.2024 DCK 2024 Kongressbericht

Seit November 2023 gibt es evidenzbasierte Empfehlungen zum perioperativen Management bei gastrointestinalen Tumoren (POMGAT) auf S3-Niveau. Vieles wird schon entsprechend der Empfehlungen durchgeführt. Wo es im Alltag noch hapert, zeigt eine Umfrage in einem Klinikverbund.

Proximale Humerusfraktur: Auch 100-Jährige operieren?

01.05.2024 DCK 2024 Kongressbericht

Mit dem demographischen Wandel versorgt auch die Chirurgie immer mehr betagte Menschen. Von Entwicklungen wie Fast-Track können auch ältere Menschen profitieren und bei proximaler Humerusfraktur können selbst manche 100-Jährige noch sicher operiert werden.

Die „Zehn Gebote“ des Endokarditis-Managements

30.04.2024 Endokarditis Leitlinie kompakt

Worauf kommt es beim Management von Personen mit infektiöser Endokarditis an? Eine Kardiologin und ein Kardiologe fassen die zehn wichtigsten Punkte der neuen ESC-Leitlinie zusammen.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.