Plasmin releases the anti-tumor peptide from the NC1 domain of collagen XIX

Oncotarget

Volumn 6, Issue 6, 2015, Pages 3656-3668

  Oudart, Jean Baptiste ^a,b   Brassart Pasco, Sylvie ^a   Vautrin, Alexia ^a   Sellier, Christèle ^a   Machado, Carine ^a   Dupont Deshorgue, Aurelie ^a   Brassart, Bertrand ^a   Baud, S ^a   Dauchez, Manuel ^a   Monboisse, Jean Claude ^a,b   Harakat, Dominique ^a   Maquart, François Xavier ^a,b   Ramont, Laurent ^a,b  

^a UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^b REIMS UNIVERSITY HOSPITAL   (France)

Author keywords

Collagen XIX; NC1 domain; Plasmin; Proteolysis; Tumor invasion; Type I turn

Indexed keywords

COLLAGEN; COLLAGEN TYPE 19; PLASMIN; UNCLASSIFIED DRUG; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOLECULAR MODEL; MOUSE; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN SECRETION; TUMOR INVASION; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CELL CULTURE TECHNIQUE; CHEMISTRY; GENETIC TRANSFECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MELANOMA; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; NEOPLASM; PATHOLOGY; PROCEDURES; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLLAGEN; FIBRINOLYSIN; HUMANS; MELANOMA; MICE, INBRED C57BL; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOPLASMS; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; TRANSFECTION;

EID: 84924231074     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2849     Document Type: Article

References (53)

1. Yurchenco PD. Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb Perspect Biol. 2011; 3:pii:a004911 doi: 10.1101/cshperspect.a004911.
2. LeBleu VS, Macdonald B, Kalluri R. Structure and function of basement membranes. Exp Biol Med (Maywood). 2007; 232:1121-1129.
3. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer. 2003; 3:422-433.
4. Suhr F, Brixius K, Bloch W. Angiogenic and vascular modulation by extracellular matrix cleavage products. Curr Pharm Des. 2009; 15:389-410.
5. Maquart FX, Siméon A, Pasco S, Monboisse JC. Regulation of cell activity by the extracellular matrix: the concept of matrikines. J Soc Biol. 1999; 193:423-428.
6. Monboisse JC, Oudart JB, Ramont L, Brassart-Pasco S, Maquart FX. Matrikines from basement membrane collagens: a new anti-cancer strategy. Biochim Biophys Acta. 2014; 1840:2589-2598.
7. Hamano Y, Zeisberg M, Sugimoto H, Lively JC, Maeshima Y, Yang C, Hynes RO, Werb Z, Sudhakar A, Kalluri R. Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell. 2003; 3:589-601.
8. Ricard-Blum S. The collagen family. Cold Spring Harb Perspect Biol. 2011; 3:a004978 doi: 10.1101/cshperspect.a004978.
9. Salant DJ. Goodpasture's disease-new secrets revealed. N Engl J Med. 2010; 363:388-91.
10. Dhar DK, Ono T, Yamanoi A, Soda Y, Yamaguchi E, Rahman MA, Kohno H, Nagasue N. Serum endostatin predicts tumor vascularity in hepatocellular carcinoma. Cancer. 2002; 95:2188-2195.
11. Luo YQ, Yao Li-Juan, Zhao L, Sun AY, Dong H, Du JP, Wu SZ, Hu W. Development of an ELISA for quantification of tumstatin in serum samples and tissue extracts of patients with lung carcinoma. Clin Chim Acta. 2010; 411:510-515.
12. Bono P, Teerenhovi L, Joensuu H. Elevated serum endostatin is associated with poor outcome in patients with non-Hodgkin lymphoma. Cancer. 2003; 97:2767-2775.
13. Kilis-Pstrusinska K, Wikiera-Magott I, Zwolinska D, Kopec W, Rzeszutko M. Analysis of collagen IV and fibronectin in blood and urine in evaluation of nephrotic fibrosis in children with chronic glomerulonephritis. Med Sci Monit. 2002; 8:CR713-719.
14. Szarvas T, László V, Vom Dorp F, Reis H, Szendröi A, Romics I, Tilki D, Rübben H, Ergün S. Serum endostatin levels correlate with enhanced extracellular matrix degradation and poor patients' prognosis in bladder cancer. Int J Cancer. 2012; 130:2922-2929.
15. Oudart JB, Brassart-Pasco S, Luczka E, Dupont-Deshorgue A, Bellon G, Boudko SP, Bächinger HP, Monboisse JC, Maquart FX, Ramont L. Analytical methods for measuring collagen XIX in human cell cultures, tissue extracts, and biological fluids. Anal Biochem. 2013; 437:111-1117.
16. Yoshioka H, Zhang H, Ramirez F, Mattei M-G, Moradi-Ameli M, van der Rest M, Gordon MK. Synteny between the loci for a novel FACIT-like collagen locus (D6S228E) and α1(IX) collagen (COL9A1) on 6q12-q14 in humans. Genomics. 1992; 13:884-886.
17. Myers JC, Sun MJ, D'Ippolito JA, Jabs EW, Neilson EG, Dion AS. Human cDNA clones transcribed from an unusually high-molecular-weight RNA encode a new collagen chain. Gene. 1993; 123:211-217.
18. Myers JC, Yang H, D'Ippolito JA, Presente A, Miller MK, Dion AS. The triple-helical region of human type XIX collagen consists of multiple collagenous subdomains and exhibits limited sequence homology to alpha 1(XVI). J Biol Chem. 1994; 269:18549-18557.
19. Sumiyoshi H, Inoguchi K, Khaleduzzaman M, Ninomiya Y, Yoshioka H. Ubiquitous expression of the alpha1(XIX) collagen gene (Col19a1) during mouse embryogenesis becomes restricted to a few tissues in the adult organism. J Biol Chem. 1997; 272:17104-17111.
20. Inoguchi K, Yoshioka H, Khaleduzzaman M, Ninomiya Y. The mRNA for α1(XIX) Collagen Chain, a New Member of FACITs, Contains a Long Unusual 3' Untranslated Region and Displays Many Unique Splicing Variants. The Journal of Biochemistry. 1995; 117:137-146.
21. Gerecke DR, Olson PF, Koch M, Knoll JH, Taylor R, Hudson DL, Champliaud MF, Olsen BR, Burgeson RE. Complete primary structure of two splice variants of collagen XII, and assignment of alpha 1(XII) collagen (COL12A1), alpha 1(IX) collagen (COL9A1), and alpha 1(XIX) collagen (COL19A1) to human chromosome 6q12-q13. Genomics. 1997; 41:236-242.
22. Khaleduzzaman M, Sumiyoshi H, Ueki Y, Inoguchi K, Ninomiya Y, Yoshioka H. Structure of the human type XIX collagen (COL19A1) gene, which suggests it has arisen from an ancestor gene of the FACIT family. Genomics. 1997; 45:304-312.
23. Myers JC, Li D, Bageris A, Abraham V, Dion AS, Amenta PS. Biochemical and immunohistochemical characterization of human type XIX defines a novel class of basement membrane zone collagens. Am J Pathol. 1997; 151:1729-1740.
24. Amenta P.S, Hadad S, Lee MT, Barnard N, Li D, Myers J.C. Loss of types XV and XIX collagen precedes basement membrane invasion in ductal carcinoma of the female breast. J. Pathol. 2003; 199:298-308.
25. Toubal A, Ramont L, Terryn C, Brassart-Pasco S, Patigny D, Sapi J, Monboisse JC, Maquart FX. The NC1 domain of type XIX collagen inhibits melanoma cell migration. Eur J Dermatol. 2010; 20:712-718.
26. Ramont L, Brassart-Pasco S, Thevenard J, Deshorgue A, Venteo L, Laronze JY, Pluot M, Monboisse JC, Maquart FX. The NC1 domain of type XIX collagen inhibits in vivo melanoma growth. Mol Cancer Ther. 2007; 6:506-514.
27. Wilman B. Primary structure of the B-chain of human plasmin. Eur J Biochem. 1977; 76:129-137.
28. Madison EL, Coombs GS, Corey DR. Substrate specificity of tissue type plasminogen activator. Characterization of the fibrin independent specificity of t-PA for plasminogen. J Biol Chem. 1995; 270:7558-7562.
29. Boudko SP, Zientek KD, Vance J, Hacker JL, Engel J, Bächinger HP. The NC2 domain of collagen IX provides chain selection and heterotrimerization. J Biol Chem. 2010; 30;285:23721-23731.
30. Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 1983; 22:2577-25637.
31. Liotta LA, Steeg PS, Stetler-Stevenson WG. Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell. 1991; 64:327-336.
32. Monboisse JC, Oudart JB, Brezillon S, Brassart B, Ramont L, Maquart FX, Brassart-Pasco S. Control of tumor progression by extracellular matrix molecule fragments, the matrikines. J Carcinogenes Mutagenes. 2013; http://dx.doi.org/10,4172/2157-2518,1000148.
33. Khatib AM, Nip J, Fallavollita L, Lehmann M, Jensen G, Brodt P. Regulation of urokinase plasminogen activator/plasmin-mediated invasion of melanoma cells by the integrin vitronectin receptor alphavbeta3. Int J Cancer. 2001; 91:300-308.
34. Meissauer A, Kramer MD, Schirrmacher V, Brunner G. Generation of cell surface-bound plasmin by cell-associated urokinase-type or secreted tissue-type plasminogen activator: a key event in melanoma cell invasiveness in vitro. Exp Cell Res. 1992; 199:179-190.
35. Fukuda H, Mochizuki S, Abe H, Okano HJ, Hara-Miyauchi C, Okano H, Yamaguchi N, Nakayama M, D'Armiento J, Okada Y. Host-derived MMP-13 exhibits a protective role in lung metastasis of melanoma cells by local endostatin production. Br J Cancer. 2011; 105:1615-1624.
36. Heljasvaara R, Nyberg P, Luostarinen J, Parikka M, Heikkilä P, Rehn M, Sorsa T, Salo T, Pihlajaniemi T. Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp Cell Res. 2005; 307:292-304.
37. Ma DH-K, Yao J-Y, Kuo M-T, See L-C, Lin K-Y, Chen S-C, Chen JK, Chao AS, Wang SF, Lin KK. Generation of endostatin by matrix metalloproteinase and cathepsin from human limbocorneal epithelial cells cultivated on amniotic membrane. Invest Ophthalmol Vis Sci. 2007; 48:644-651.
38. Felbor U, Dreier L, Bryant RA, Ploegh HL, Olsen BR, Mothes W. Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J. 2000; 19:1187-1194.
39. Veillard F, Saidi A, Burden RE, Scott CJ, Gillet L, Lecaille F, Lalmanach G. Cysteine cathepsins S and L modulate anti-angiogenic activities of human endostatin. J Biol Chem. 2011; 286:37158-37167.
40. O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997; 88:277-285.
41. Chen H, Xue L-X, Cao H-L, Chen S-W, Guo Y, Gao WW, Ju SM, Tian HL. Endostatin/collagen XVIII is increased in cerebrospinal fluid after severe traumatic brain injury. Biomed Res Int. 2013; 2013:402375.
42. Andreasen PA, Egelund R, Petersen HH. The plasminogen activation system in tumor growth, invasion, and metastasis. Cell Mol Life Sci. 2000; 57:25-40.
43. De Vries TJ, van Muijen GN, Ruiter DJ. The plasminogen activation system in melanoma cell lines and in melanocytic lesions. Melanoma Res. 1996; 6:79-88.
44. Lauer-Fields JL, Sritharan T, Stack MS, Nagase H, Fields GB. Selective hydrolysis of triple-helical substrates by matrix metalloproteinase-2 and-9. J Biol Chem. 2003; 278:18140-1815.
45. Lauer-Fields JL, Tuzinski KA, Shimokawa Ki, Nagase H, Fields GB. Hydrolysis of triple-helical collagen peptide models by matrix metalloproteinases. J Biol Chem. 2000; 275:13282-13290.
46. Thevenard J, Floquet N, Ramont L, Prost E, Nuzillard J-M, Dauchez M, Yezid H, Alix AJ, Maquart FX, Monboisse JC, Brassart-Pasco S. Structural and antitumor properties of the YSNSG cyclopeptide derived from tumstatin. Chem Biol. 2006; 13:1307-1315.
47. Thevenard J, Ramont L, Devy J, Brassart B, Dupont-Deshorgue A, Floquet N, Schneider L, Ouchani F, Terryn C, Maquart FX, Monboisse JC, Brassart-Pasco S. The YSNSG cyclopeptide derived from tumstatin inhibits tumor angiogenesis by down-regulating endothelial cell migration. Int J Cancer. 2010; 126:1055-1066.
48. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJC. GROMACS: fast, flexible, and free. J Comput Chem. 2005; 26:1701-1718.
49. Jorgensen WL, Tiradorives J. The Opls Potential Functions for Proteins-Energy Minimizations for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 1998; 110:1657-1666.
50. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 2008; 9:40.
51. Maupetit J, Derreumaux P, Tufféry P. A fast method for large-scale de novo peptide and miniprotein structure prediction. J Comput Chem. 2010; 31:726-738.
52. Maupetit J, Derreumaux P, Tufféry P. PEP-FOLD: an online resource for de novo peptide structure prediction. Nucleic Acids Res. 2009; 37:W498-503.
53. Thévenet P, Shen Y, Maupetit J, Guyon F, Derreumaux P, Tufféry P. PEP-FOLD: an updated de novo structure prediction server for both linear and disulfide bonded cyclic peptides. Nucleic Acids Res. 2012; 40:W288-93.