SIKVAV, a laminin α1-derived peptide, interacts with integrins and increases protease activity of a human salivary gland adenoid cystic carcinoma cell line through the ERK 1/2 signaling pathway

American Journal of Pathology

Volumn 171, Issue 1, 2007, Pages 124-138

  Freitas, Vanessa M ^a   Vilas Boas, Vanessa F ^a   Pimenta, Daniel C ^b   Loureiro, Vania ^c   Juliano, Maria A ^d   Carvalho, Márcia R ^e   Pinheiro, João J V ^e   Camargo, Antonio C M ^b   Moriscot, Anselmo S ^a   Hoffman, Matthew P ^f   Jaeger, Ruy G ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

^c UNIVERSIDADE METROPOLITANA DE SANTOS   (Brazil)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^e University of Para   (Brazil)

^f NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA3 INTEGRIN; ALPHA6 INTEGRIN; BETA1 INTEGRIN; BINDING PROTEIN; GELATINASE A; GELATINASE B; INTEGRIN; ISOLEUCYLVALYLSERYLLYSYLVALYLALANINE; LAMININ ALPHA 1; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEINASE; SERYLISOLEUCYLLYSYLVALYLALANYLVALINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 3; VERY LATE ACTIVATION ANTIGEN 6; LAMININ; LAMININ A; MATRIX METALLOPROTEINASE; OLIGOPEPTIDE; SERYL ISOLEUCYL LYSYL VALYL ALANYL VALINAMIDE; SERYL-ISOLEUCYL-LYSYL-VALYL-ALANYL-VALINAMIDE;

ADENOID CYSTIC CARCINOMA; AFFINITY CHROMATOGRAPHY; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME RELEASE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOLOCALIZATION; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; SALIVARY GLAND CARCINOMA; SIGNAL TRANSDUCTION; ZYMOGRAPHY; CELL CULTURE; METABOLISM; SALIVARY GLAND TUMOR;

ANTIGENS, CD29; CARCINOMA, ADENOID CYSTIC; HUMANS; INTEGRIN ALPHA6; INTEGRINS; LAMININ; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; OLIGOPEPTIDES; SALIVARY GLAND NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 34547654434     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.051264     Document Type: Article

References (69)

1. Seifert G, Sobin LH: The World Health Organization's Histological Classification of Salivary Gland Tumors: a commentary on the second edition. Cancer 1992, 70:379-385
2. Dardick I: Salivary Gland Tumor Pathology. New York, Igaku-Shoin, 1996
3. Loducca SV, Raitz R, Araujo NS, Araujo VC: Polymorphous low-grade adenocarcinoma and adenoid cystic carcinoma: distinct architectural composition revealed by collagen IV, laminin and their integrin ligands (α2β1 and γ3β1). Histopathology 2000, 37:118-123
4. Cheng J, Irie T, Munakata R, Kimura S, Nakamura H, He RG, Lui AR, Saku T: Biosynthesis of basement membrane molecules by salivary adenoid cystic carcinoma cells: an immunofluorescence and confocal microscopic study. Virchows Arch 1995, 426:577-586
5. Cheng J, Saku T, Okabe H, Furthmayr H: Basement membranes in adenoid cystic carcinoma. An immunohistochemical study. Cancer 1992, 69:2631-2640
6. Raitz R, Martins MD, Araujo VC: A study of the extracellular matrix in salivary gland tumors. J Oral Pathol Med 2003, 32:290-296
7. Capuano AC, Jaeger RG: The effect of laminin and its peptide SIKVAV on a human salivary gland myoepithelioma cell line. Oral Oncol 2004, 40:36-42
8. de Oliveira PT, Jaeger MM, Miyagi SP, Jaeger RG: The effect of a reconstituted basement membrane (matrigel) on a human salivary gland myoepithelioma cell line. Virchows Arch 2001, 439:571-578
9. França CM, Jaeger MM, Jaeger RG, Araujo NS: The role of basement membrane proteins on the expression of neural cell adhesion molecule (N-CAM) in an adenoid cystic carcinoma cell line. Oral Oncol 2000, 36:248-252
10. França CM, Jaeger RG, Freitas VM, Araujo NS, Jaeger MM: Effect of N-CAM on in vitro invasion of human adenoid cystic carcinoma cells. Oral Oncol 2001, 37:638-642
11. Freitas VM, Jaeger RG: The effect of laminin and its peptide SIKVAV on a human salivary gland adenoid cystic carcinoma cell line. Virchows Arch 2002, 441:569-576
12. Freitas VM, Scheremeta B, Hoffman MP, Jaeger RG: Laminin-1 and SIKVAV a laminin-1-derived peptide, regulate the morphology and protease activity of a human salivary gland adenoid cystic carcinoma cell line. Oral Oncol 2004, 40:483-489
13. Jaeger MM, Araujo VC, Kachar B, Jaeger RG: Effect of spatial arrangement of the basement membrane on cultured pleomorphic adenoma cells: study by immunocytochemistry and electron and confocal microscopy. Virchows Arch 1997, 430:467-477
14. Jaeger RG, de Oliveira PT, Jaeger MM, de Araujo VC: Expression of smooth-muscle actin in cultured cells from human plasmacytoid myoepithelioma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997, 84:663-667
15. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, Engel J, Engvall E, Hohenester E, Jones JC, Kleinman HK, Marinkovich MP, Martin GR, Mayer U, Meneguzzi G, Miner JH, Miyazaki K, Patarroyo M, Paulsson M, Quaranta V, Sanes JR, Sasaki T, Sekiguchi K, Sorokin LM, Talts JF, Tryggvason K, Uitto J, Virtanen I, von der Mark K, Wewer UM, Yamada Y, Yurchenco PD: A simplified laminin nomenclature. Matrix Biol 2005, 24:326-332
16. Ekblom P: Extracellular matrix and cell adhesion molecules in nephrogenesis. Exp Nephrol 1996, 4:92-96
17. Kleinman HK, Philp D, Hoffman MP: Role of the extracellular matrix in morphogenesis. Curr Opin Biotechnol 2003, 14:526-532
18. Faisal Khan KM, Laurie GW, McCaffrey TA, Falcone DJ: Exposure of cryptic domains in the alpha 1-chain of laminin-1 by elastase stimulates macrophages urokinase and matrix metalloproteinase-9 expression. J Biol Chem 2002, 277:13778-13786
19. Mott JD, Werb Z: Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 2004, 16:558-564
20. Schenk S, Quaranta V: Tales from the crypt[ic] sites of the extracellular matrix. Trends Cell Biol 2003, 13:366-375
21. Davis GE, Bayless KJ, Davis MJ, Meininger GA: Regulation of tissue injury responses by the exposure of matricryptic sites within extracellular matrix molecules. Am J Pathol 2000, 156:1489-1498
22. Corcoran ML, Kibbey MC, Kleinman HK, Wahl LM: Laminin SIKVAV peptide induction of monocyte/macrophage prostaglandin E2 and matrix metalloproteinases. J Biol Chem 1995, 270:10365-10368
23. Grant DS, Kinsella JL, Fridman R, Auerbach R, Piasecki BA, Yamada Y, Zain M, Kleinman HK: Interaction of endothelial cells with a laminin A chain peptide (SIKVAV) in vitro and induction of angiogenic behavior in vivo. J Cell Physiol 1992, 153:614-625
24. Khan KM, Falcone DJ: Selective activation of MAPK(erk1/2) by laminin-1 peptide alpha1:Ser: (2091)-Arg(2108) regulates macrophage degradative phenotype. J Biol Chem 2000, 275:4492-4498
25. Kibbey MC, Grant DS, Kleinman HK: Role of the SIKVAV site of laminin in promotion of angiogenesis and tumor growth: an in vivo Matrigel model. J Natl Cancer Inst 1992, 84:1633-1638
26. Royce LS, Martin GR, Kleinman HK: Induction of an invasive phenotype in benign tumor cells with a laminin A-chain synthetic peptide. Invasion Metastasis 1992, 12:149-155
27. Sephel GC, Tashiro KI, Sasaki M, Greatorex D, Martin GR, Yamada Y, Kleinman HK: Laminin A chain synthetic peptide which supports neurite outgrowth. Biochem Biophys Res Commun 1989, 162:821-829
28. Shintani S, Alcalde RE, Matsumura T, Terakado N: Extracellular matrices expression in invasion area of adenoid cystic carcinoma of salivary glands. Cancer Lett 1997, 116:9-14
29. Kasai S, Ohga Y, Mochizuki M, Nishi N, Kadoya Y, Nomizu M: Multifunctional peptide fibrils for biomedical materials. Biopolymers 2004, 76:27-33
30. Almiñana N, Grau-Oliete MR, Reig F, Rivera-Fillat MP: In vitro effects of SIKVAV retro and retro-enantio analogues on tumor metastatic events. Peptides 2004, 25:251-259
31. Almiñana N, Alsina MA, Espina M, Reig F: Synthesis and physicochemical study of the laminin active sequence: SIKVAV. J Colloid Interface Sci 2003, 263:432-440
32. Hashimoto T, Suzuki Y, Tanihara M, Kakimaru Y, Suzuki K: Development of alginate wound dressings linked with hybrid peptides derived from laminin and elastin. Biomaterials 2004, 25:1407-1414
33. Tong YW, Shoichet MS: Enhancing the neuronal interaction on fluoropolymer surfaces with mixed peptides or spacer group linkers. Biomaterials 2001, 22:1029-1034
34. Grant DS, Zukowska Z: Revascularization of ischemic tissues with SIKVAV and neuropeptide Y (NPY). Adv Exp Med Biol 2000, 476:139-154
35. Hogervorst F, Admiraal LG, Niessen C, Kuikman I, Janssen H, Daams H, Sonnenberg A: Biochemical characterization and tissue distribution of the A and B variants of the integrin α6 subunit. J Cell Biol 1993, 121:179-191
36. Nagata M, Fujita H, Ida H, Hoshina H, Inoue T, Seki Y, Ohnishi M, Ohyama T, Shingaki S, Kaji M, Saku T, Takagi R: Identification of potential biomarkers of lymph node metastasis in oral squamous cell carcinoma by cDNA microarray analysis. Int J Cancer 2003, 106:683-689
37. Stossi F, Barnett DH, Frasor J, Komm B, Lyttle CR, Katzenellenbogen BS: Transcriptional profiling of estrogen-regulated gene expression via estrogen receptor (ER) α or ERβ in human osteosarcoma cells: distinct and common target genes for these receptors. Endocrinology 2004, 145:3473-3486
38. Sun H, Berquin IM, Edwards IJ: Omega-3 polyunsaturated fatty acids regulate syndecan-1 expression in human breast cancer cells. Cancer Res 2005, 65:4442-4447
39. Lim H, Eng J, Yates 3rd JR, Tollaksen SL, Giometti CS, Holden JF, Adams MW, Reich CI, Olsen GJ, Hays LG: Identification of 2D-gel proteins: a comparison of MALDI/TOF peptide mass mapping to μ LC-ESI tandem mass spectrometry. J Am Soc Mass Spectrom 2003, 14:957-970
40. Linder S, Kopp P: Podosomes at a glance. J Cell Sci 2005, 118:2079-2082
41. Linder S, Aepfelbacher M: Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol 2003, 13:376-385
42. Kadoya Y, Yamashina S: Salivary gland morphogenesis and basement membranes. Anat Sci Int 2005, 80:71-79
43. Kuratomi Y, Nomizu M, Tanaka K, Ponce ML, Komiyama S, Kleinman HK, Yamada Y: Laminin γ1 chain peptide, C-16 (KAFDITYVRLKF), promotes migration, MMP-9 secretion, and pulmonary metastasis of B16-F10 mouse melanoma cells. Br J Cancer 2002, 86:1169-1173
44. Skubitz AP, McCarthy JB, Zhao Q, Yi XY, Furcht LT: Definition of a sequence, RYVVLPR, within laminin peptide F-9 that mediates metastatic fibrosarcoma cell adhesion and spreading. Cancer Res 1990, 50:7612-7622
45. Iwamoto Y, Robey FA, Graf J, Sasaki M, Kleinman HK, Yamada Y, Martin GR: YIGSR, a synthetic laminin pentapeptide, inhibits experimental metastasis formation. Science 1987, 238:1132-1134
46. Hoffman MP, Nomizu M, Roque E, Lee S, Jung DW, Yamada Y, Kleinman HK: Laminin-1 and laminin-2 G-domain synthetic peptides bind syndecan-1 and are involved in acinar formation of a human submandibular gland cell line. J Biol Chem 1998, 273:28633-28641
47. Charonis AS, Skubitz AP, Koliakos GG, Reger LA, Dege J, Vogel AM, Wohlhueter R, Furcht LT: A novel synthetic peptide from the B1 chain of laminin with heparin-binding and cell adhesion-promoting activities. J Cell Biol 1988, 107:1253-1260
48. Graf J, Ogle RC, Robey FA, Sasaki M, Martin GR, Yamada Y, Kleinman HK: A pentapeptide from the laminin B1 chain mediates cell adhesion and binds the 67,000 laminin receptor. Biochemistry 1987, 26:6896-6900
49. Kanemoto T, Reich R, Royce L, Greatorex D, Adler SH, Shiraishi N, Martin GR, Yamada Y, Kleinman HK: Identification of an amino acid sequence from the laminin A chain that stimulates metastasis and collagenase IV production. Proc Natl Acad Sci USA 1990, 87:2279-2283
50. Kleinman HK, Graf J, Iwamoto Y, Sasaki M, Schasteen CS, Yamada Y, Martin GR, Robey FA: Identification of a second active site in laminin for promotion of cell adhesion and migration and inhibition of in vivo melanoma lung colonization. Arch Biochem Biophys 1989, 272:39-45
51. Kuratomi Y, Nomizu M, Nielsen PK, Tanaka K, Song SY, Kleinman HK, Yamada Y: Identification of metastasis-promoting sequences in the mouse laminin α1 chain. Exp Cell Res 1999, 249:386-395
52. Tashiro K, Sephel GC, Weeks B, Sasaki M, Martin GR, Kleinman HK, Yamada Y: A synthetic peptide containing the IKVAV sequence from the A chain of laminin mediates cell attachment, migration, and neurite outgrowth. J Biol Chem 1989, 264:16174-16182
53. Nomizu M, Kuratomi Y, Malinda KM, Song SY, Miyoshi K, Otaka A, Powell SK, Hoffman MP, Kleinman HK, Yamada Y: Cell binding sequences in mouse laminin α1 chain. J Biol Chem 1998, 273:32491-32499
54. Nomizu M, Kuratomi Y, Ponce ML, Song SY, Miyoshi K, Otaka A, Powell SK, Hoffman MP, Kleinman HK, Yamada Y: Cell adhesive sequences in mouse laminin β1 chain. Arch Biochem Biophys 2000, 378:311-320
55. Nomizu M, Kuratomi Y, Song SY, Ponce ML, Hoffman MP, Powell SK, Miyoshi K, Otaka A, Kleinman HK, Yamada Y: Identification of cell binding sequences in mouse laminin gamma1 chain by systematic peptide screening. J Biol Chem 1997, 272:32198-32205
56. Iwamoto Y, Graf J, Sasaki M, Kleinman HK, Greatorex DR, Martin GR, Robey FA, Yamada Y: Synthetic pentapeptide from the B1 chain of laminin promotes B16F10 melanoma cell migration. J Cell Physiol 1988, 134:287-291
57. Nomizu M, Utani A, Shiraishi N, Kibbey MC, Yamada Y, Roller PP: The all-D-configuration segment containing the IKVAV sequence of laminin A chain has similar activities to the all-L-peptide in vitro and in vivo. J Biol Chem 1992, 267:14118-14121
58. Khan KM, Falcone DJ: Role of laminin in matrix induction of macrophage urokinase-type plasminogen activator and 92-kDa metalloproteinase expression. J Biol Chem 1997, 272:8270-8275
59. Hynes RO: Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992, 69:11-25
60. Mercurio AM: Laminin receptors: achieving specificity through cooperation. Trends Cell Biol 1995, 5:419-423
61. Wu CC, Mao Coss MJ, Howell KE, Yates III JR: A method for the comprehensive proteomic analysis of membrane proteins. Nat Biotechnol 2003, 21:532-538
62. Kleinman HK, Weeks BS, Cannon FB, Sweeney TM, Sephel GC, Clement B, Zain M, Olson MO, Jucker M, Burrous BA: Identification of a 110-kDa nonintegrin cell surface laminin-binding protein which recognizes an A chain neurite-promoting peptide. Arch Biochem Biophys 1991, 290:320-325
63. Engbring JA, Hoffman MP, Karmand AJ, Kleinman HK: The B16F10 cell receptor for a metastasis-promoting site on laminin-1 is a heparan sulfate/chondroitin sulfate-containing proteoglycan. Cancer Res 2002, 62:3549-3554
64. Morgan MR, Thomas GJ, Russell A, Hart IR, Marshall JF: The integrin cytoplasmic-tail motif EKQKVDLSTDC is sufficient to promote tumor cell invasion mediated by matrix metalloproteinase (MMP)-2 or MMP-9. J Biol Chem 2004, 279:26533-26539
65. Davidson B, Goldberg I, Gotlieb WH, Kopolovic J, Risberg B, Ben-Baruch G, Reich R: Coordinated expression of integrin subunits, matrix metalloproteinases (MMP), angiogenic genes and Ets transcription factors in advanced-stage ovarian carcinoma: a possible activation pathway? Cancer Metastasis Rev 2003, 22:103-115
66. Giannelli G, Bergamini C, Fransvea E, Marinosci F, Quaranta V, Antonaci S: Human hepatocellular carcinoma (HCC) cells require both alpha3beta1 integrin and matrix metalloproteinases activity for migration and invasion. Lab Invest 2001, 81:613-627
67. Ghosh S, Stack MS: Proteolytic modification of laminins: functional consequences. Microsc Res Tech 2000, 51:238-246
68. Paulsson M, Deutzmann R, Timpl R, Dalzoppo D, Odermatt E, Engel J: Evidence for coiled-coil α-helical regions in the long arm of laminin. EMBO J 1985, 4:309-316
69. Miner JH, Yurchenco PD: Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 2004, 20:255-284