Inflammopharmacology

, Volume 19, Issue 3, pp 117–129 | Cite as

Lysyl oxidase: a potential target for cancer therapy

  • Siddikuzzaman
  • V. M. Berlin Grace
  • C. Guruvayoorappan
Review

Abstract

Lysyl oxidases (LysOX; EC 1.4.3.13, protein-lysine 6-oxidases) are extracellular copper enzymes that catalyze the cross-linking of collagens or elastin in the extracellular matrix (ECM), thereby regulating the tensile strength of tissues. Recent implication of LysOX in cancer, wound healing, cell motility, chemotaxis, and differentiation reflects its remarkable functional diversity and also in the central nervous system pathologies. However, recent reports also demonstrated novel roles for LysOX, including the ability to regulate gene transcription, motility/migration, and cell adhesion. These diverse functions have led researchers to hypothesize that LysOX may have multiple roles affecting both extra- and intracellular cell function(s). Both down and up-regulation of LysOX in tumor tissues and cancer cell lines have been described, suggesting a dual role for LysOX as a tumor suppressor, as well as a metastasis promoter gene. In this review we explain in detail the role of lysyl oxidase in tumor progression and metastasis.

Keywords

Lysyl oxidase Copper Extra cellular matrix Cancer Tumor suppressor Metastasis promoter 

Notes

Acknowledgments

The Valuable support of Dr. Patrick Gomez, Director, School of Biotechnology and Health Sciences, Karunya University is greatfully acknowledged.

References

  1. Akiri G, Sabo E, Dafni H, Vadasz Z, Kartvelishvily Y, Gan N, Kessler O, Cohan T, Resnick M, Neeman M, Neufeld G (2003) Lysyl oxidase-related protein-1 promotes tumor fibrosis and tumor progression in vivo. Cancer Res 63:1657–1666PubMedGoogle Scholar
  2. Bailey AJ (2001) Molecular mechanisms of ageing in connective tissues. Mech Ageing Dev 122:735–755PubMedCrossRefGoogle Scholar
  3. Barry-Hamilton V, Spangler R, Marshal LD, McCauley S, Rodriguez HM, Oyasu M, Mikels A, Vaysberg M, Ghermazien H, Wai C, Garcia CA, Velayo AC, Jorgensen B, Biermann D, Tsai D, Green J, Zaffryar-Eilot S, Holzer A, Ogg S, Thai D, Neufeld G, Van VP, Smith V (2010) Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med 16(9):1009–1017PubMedCrossRefGoogle Scholar
  4. Bateman JF, Cole WG, Pillow JJ, Ramshaw JA (1986) Induction of procollagen processing in fibroblast cultures by neutral polymers. J Biol Chem 261:4198–4203PubMedGoogle Scholar
  5. Boak AM, Roy R, Berk J, Taylor L, Polgar P, Goldstein RH, Kagan HM (1994) Regulation of lysyl oxidase expression in lung fibroblasts by transforming growth factor-beta 1 and prostaglandin E2. Am J Respir Cell Mol Biol 11:751–755PubMedGoogle Scholar
  6. Borczuk AC, Kim HK, Yegen HA, Friedman RA, Powell CA (2005) Lung adenocarcinoma global profiling identifies type II transforming growth factor-beta receptor as a repressor of invasiveness. Am J Respir Crit Care Med 172(6):729–737PubMedCrossRefGoogle Scholar
  7. Bose KK, Chakraborty J, Khuder S, Smith-Mensah WH, Robinson J (2000) Lysyl oxidase activity in the cells of flexor retinaculum of individuals with carpal tunnel syndrome. J Occup Environ Med 42:582–587PubMedCrossRefGoogle Scholar
  8. Bouez C, Reynaud C, Noblesse E, Thepot A, Gleyzal C, Kanitakis J, Perrier E, Damour O, Sommer P (2006) The lysyl oxidase LOX is absent in basal and squamous cell carcinomas and its knockdown induces an invading phenotype in a skin equivalent model. Clin Cancer Res 12(5):1463–1469PubMedCrossRefGoogle Scholar
  9. Boyd CD, Mariani TJ, Kim Y, Csiszar K (1995) The size heterogeneity of human lysyl oxidase mRNA is due to alternate polyadenylation site and not alternate exon usage. Mol Biol Rep 21:95–103PubMedCrossRefGoogle Scholar
  10. Bronson RE, Calaman SD, Traish AM, Kagan HM (1987) Stimulation of lysyl oxidase (EC 1.4.3.13) activity by testosterone and characterization of androgen receptors in cultured calf aorta smooth-muscle cells. Biochem J 244:317–323PubMedGoogle Scholar
  11. Buchinger B, Spitzer S, Karlic H, Klaushofer K, Varga F (2008) Lysyl oxidase (LOX) mRNA expression and genes of the differentiated osteoblastic phenotype are upregulated in human osteosarcoma cells by suramin. Cancer Lett 265(1):45–54PubMedCrossRefGoogle Scholar
  12. Byers PH (2001) Folding defects in fibrillar collagens. Philos Trans R Soc Lond B Biol Sci 356:151–157PubMedCrossRefGoogle Scholar
  13. Byers PH, Siegel RC, Holbrook KA, Narayanan AS, Bornstein P, Hall JG (1980) X-linked cutis laxa: defective cross-link formation in collagen due to decreased lysyl oxidase activity. N Engl J Med 303:61–65PubMedCrossRefGoogle Scholar
  14. Carlotta G, Tiziana F, Janine TE, Amato JG, Marco M, Filippo M (2009) Bioreductively activated lysyl oxidase inhibitors against hypoxic tumours. ChemMedChem 4:1590–1594CrossRefGoogle Scholar
  15. Casey ML, MacDonald PC (1997) Lysyl oxidase (ras recision gene) expression in human amnion: ontogeny and cellular localization. J Clin Endocrinol Metab 82:167–172PubMedCrossRefGoogle Scholar
  16. Chang YS, Svinarich DM, Yang TP, Krawetz SA (1993) The mouse lysyl oxidase gene (Lox) resides on chromosome 18. Cytogenet Cell Genet 63:47–49PubMedCrossRefGoogle Scholar
  17. Chanoki M, Ishii M, Kobayashi H, Fushida H, Yashiro N, Hamada T, Ooshima A (1995) Increased expression of lysyl oxidase in skin with scleroderma. Br J Dermatol 133:710–715PubMedCrossRefGoogle Scholar
  18. Choung J, Taylor L, Thomas K, Zhou X, Kagan H, Yang X, Polgar P (1998) Role of EP2 receptors and cAMP in prostaglandin E2 regulated expression of type I collagen alpha1, lysyl oxidase, and cycloox ygenase-1 genes in human embryo lung fibroblasts. J Cell Biochem 71:254–263PubMedCrossRefGoogle Scholar
  19. Chung CH, Parker JS, Ely K, Carter J, Yi Y, Murphy BA, Ang KK, El-Naggar AK, Zanation M, Cmelak AJ, Levy S, Slebos RJ, Yarbrough WG (2006) Gene expression profiles identify epithelial-to-mesenchymal transition and activation of nuclear factor-kB signaling as characteristics of a high-risk head and neck squamous cell carcinoma. Cancer Res 66:8210–8218PubMedCrossRefGoogle Scholar
  20. Colpaert C, Vermeulen P, Van Marck E, Dirix L (2001) The presence of a fibrotic focus is an independent predictor of early metastasis in lymph node-negative breast cancer patients. Am J Surg Pathol 25:1557PubMedCrossRefGoogle Scholar
  21. Contente S, Kenyon K, Rimoldi D, Friedman RM (1990) Expression of gene rrg is associated with reversion of NIH 3T3 transformed by LTR-c-H-ras. Science 249:796–798PubMedCrossRefGoogle Scholar
  22. Contente S, Csiszar K, Kenyon K, Friedman RM (1993) Structure of the mouse lysyl oxidase gene. Genomics 16:395–400PubMedCrossRefGoogle Scholar
  23. Cristina R, José MG, Berta R, Javier FA, Anna G, Lina B (2008) Regulation of lysyl oxidase in vascular cells: lysyl oxidase as a new player in cardiovascular diseases. Cardiovasc Res 79(1):7–13Google Scholar
  24. Cristina R, José MG, Berta R, Javier FA, Anna G, Sonia SG, Lina B (2009) Statins normalize vascular lysyl oxidase down-regulation induced by proatherogenic risk factors. Cardiovasc Res 83(3):595–603Google Scholar
  25. Cronlund AL, Kagan HM (1986) Comparison of lysyl oxidase from bovine lung and aorta. Connect Tissue Res 15:173–185PubMedCrossRefGoogle Scholar
  26. Cronshaw AD, Fothergill-Gilmore LA, Hulmes DJ (1995) The proteolytic processing site of the precursor of lysyl oxidase. Biochem J 306:279–284PubMedGoogle Scholar
  27. Csiszar K (2001) Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol 70:1–32PubMedCrossRefGoogle Scholar
  28. Csiszar K, Entersz I, Trackman PC, Samid D, Boyd CD (1996) Functional analysis of the promoter and first intron of the human lysyl oxidase gene. Mol Biol Rep 23(2):97–108PubMedCrossRefGoogle Scholar
  29. Csiszar K, Fong SF, Ujfalusi A, Krawetz SA, Salvati EP, Mackenzie JW, Boyd CD (2002) Somatic mutations of the lysyl oxidase gene on chromosome 5q23.1 in colorectal tumors. Int J Cancer 97(5):636–642PubMedCrossRefGoogle Scholar
  30. Debelle L, Tamburro AM (1999) Elastin: molecular description and function. Int J Biochem Cell Biol 31:261–272PubMedCrossRefGoogle Scholar
  31. Decitre M, Gleyzal C, Raccurt M, Peyrol S, Aubert-Foucher E, Csiszar K, Sommer P (1998) Lysyl oxidase-like protein localizes to sites of de novo fibrinogenesis in fibrosis and in the early stromal reaction of ductal breast carcinomas. Lab Invest 78:143–151PubMedGoogle Scholar
  32. Di Donato A, Lacal JC, Di Duca M, Giampuzzi M, Ghiggeri G, Gusmano R (1997) Micro-injection of recombinant lysyl oxidase blocks oncogenic p21-Ha-Ras and progesterone effects on Xenopus laevis oocyte maturation. FEBS Lett 419(1):63–68PubMedCrossRefGoogle Scholar
  33. Duffy MJ, Maguire TM, Hill A, McDermott E, O’Higgins N (2000) Metalloproteinases: role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res 2:252–257PubMedCrossRefGoogle Scholar
  34. Ellenrieder V, Alber B, Lacher U, Hendler SF, Menke A, Boeck W, Wagner M, Wilda M, Friess H, Buchler M, Adler G, Gress TM (2000) Role of MT-MMPs and MMP-2 in pancreatic cancer progression. Int J Cancer 85:14–20PubMedCrossRefGoogle Scholar
  35. Erler JT, Bennewith KL, Nicolau M, Dornhofer N, Kong C, Le QT, Chi JT, Jeffrey SS, Giaccia AJ (2006) Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440(7088):1222–1226PubMedCrossRefGoogle Scholar
  36. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A, Le QT, Giaccia AJ (2009) Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15(1):35–44PubMedCrossRefGoogle Scholar
  37. Faina R, Frederick TG (2010) Modeling Cu(II) binding to peptides using the extensible systematic force field. Bioinorgan Chem Appl 2010:724210. doi: 10.1155/2010/724210 Google Scholar
  38. Feres-Filho EJ, Choi YJ, Han X, Takala TE, Trackman PC (1995) Pre- and post-translational regulation of lysyl oxidase by transforming growth factor-beta 1 in osteoblastic MC3T3-E1 cells. J Biol Chem 270:30797–30803PubMedCrossRefGoogle Scholar
  39. Feres-Filho EJ, Menassa GB, Trackman PC (1996) Regulation of lysyl oxidase by basic fibroblast growth factor in osteoblastic MC3T3-E1 cells. J Biol Chem 271:6411–6416PubMedCrossRefGoogle Scholar
  40. Fitzgerald J, Morgelin M, Selan C, Wiberg C, Keene DR, Lamande SR, Bateman JF (2001) The N-terminal N5 subdomain of the alpha 3(VI) chain is important for collagen VI microfibril formation. J Biol Chem 276:187–193PubMedCrossRefGoogle Scholar
  41. Fogelgren B, Polgar N, Szauter KM, Ujfaludi Z, Laczko R, Fong KS, Csiszar K (2005) Cellular fibronectin binds to lysyl oxidase with high affinity and is critical for its proteolytic activation. J Biol Chem 280:24690–24697PubMedCrossRefGoogle Scholar
  42. Freije WA, Castro-Vargas FE, Fang Z, Horvath S, Cloughesy T, Liau LM, Mischel PS, Nelson SF (2004) Gene expression profiling of gliomas strongly predicts survival. Cancer Res 64(18):6503–6510PubMedCrossRefGoogle Scholar
  43. Fuchs B, Zhang K, Bolander ME, Sarkar G (2000) Identification of differentially expressed genes by mutually subtracted RNA fingerprinting. Anal Biochem 286(1):91–98PubMedCrossRefGoogle Scholar
  44. Fushida-Takemura H, Fukuda M, Maekawa N, Chanoki M, Kobayashi H, Yashiro N, Ishii M, Hamada T, Otani S, Ooshima A (1996) Detection of lysyl oxidase gene expression in rat skin during wound healing. Arch Dermatol Res 288:7–10PubMedCrossRefGoogle Scholar
  45. Gacheru SN, Thomas KM, Murray SA, Csiszar K, Smith-Mungo LI, Kagan HM (1997) Transcriptional and post-transcriptional control of lysyl oxidase expression in vascular smooth muscle cells: effects of TGF-beta 1 and serum deprivation. J Cell Biochem 65:395–407PubMedCrossRefGoogle Scholar
  46. Giampuzzi M, Botti G, Di Duca M, Arata L, Ghiggeri G, Gusmano R, Ravazzolo R, Di Donato A (2000) Lysyl oxidase activates the transcription activity of human collagen III promoter: possible involvement of Ku antigen. J Biol Chem 275:36341–36349PubMedCrossRefGoogle Scholar
  47. Giampuzzi M, Botti G, Cilli M, Gusmano R, Borel A, Sommer P, Di Donato A (2001) Down-regulation of lysyl oxidase-induced tumorigenic transformation in NRK-49F cells characterized by constitutive activation of ras proto-oncogene. J Biol Chem 276:29226–29232PubMedCrossRefGoogle Scholar
  48. Giampuzzi M, Oleggin R, Di Donato A (2003a) Demonstration of in vitro interaction between tumor suppressor lysyl oxidase and histones H1 and H2: definition of the regions involved. Biochim Biophys Acta 1647:245–251PubMedGoogle Scholar
  49. Giampuzzi M, Oleggini R, Di Donato A (2003b) Altered adhesion features and signal transduction in NRK-49F cells transformed by down-regulation of lysyl oxidase. Biochim Biophys Acta 1647:239–244PubMedGoogle Scholar
  50. Giampuzzi M, Oleggini R, Albanese C, Pestell R, Di Donato A (2005) β-catenin signaling and regulation of cyclin D1 promoter in NRK-49F cells transformed by down-regulation of the tumor suppressor lysyl oxidase. Biochim Biophys Acta 1745:370–381PubMedCrossRefGoogle Scholar
  51. Gibson MA, Hatzinikolas G, Kumaratilake JS, Sandberg LB, Nicholl JK, Sutherland GR, Cleary EG (1996) Further characterization of proteins associated with elastic fiber microfibrils including the molecular cloning of MAGP-2 (MP25). J Biol Chem 271:1096–1103PubMedCrossRefGoogle Scholar
  52. Green RS, Lieb ME, Weintraub AS, Gacheru SN, Rosenfield CL, Shah S, Kagan HM, Taubman MB (1995) Identification of lysyl oxidase and other platelet-derived growth factor-inducible genes in vascular smooth muscle cells by differential screening. Lab Invest 73:476–482PubMedGoogle Scholar
  53. Guruvayoorappan C, Kuttan G (2007) Beta-carotene inhibits tumor-specific angiogenesis by altering the cytokine profile and inhibits the nuclear translocation of transcription factors in B16F-10 melanoma cells. Integr Cancer Ther 6:258–270PubMedCrossRefGoogle Scholar
  54. Guruvayoorappan C, Kuttan G (2008a) Biophytum sensitivum (L.) DC inhibits tumor cell invasion and metastasis through a mechanism involving regulation of MMPs, prolyl hydroxylase, lysyl oxidase, nm23, ERK-1, ERK-2, STAT-1, and proinflammatory cytokine gene expression in metastatic lung tissue. Integr Cancer Ther 7:42–50PubMedCrossRefGoogle Scholar
  55. Guruvayoorappan C, Kuttan G (2008b) Amentoflavone inhibits experimental tumor metastasis through a regulatory mechanism involving MMP-2, MMP-9, prolyl hydroxylase, lysyl oxidase, VEGF, ERK-1, ERK-2, STAT-1, NM23 and cytokines in lung tissues of C57BL/6 mice. Immunopharmacol Immunotoxicol 30:711–727PubMedCrossRefGoogle Scholar
  56. Hajnal A, Klemenz R, Schafer R (1993) Up-regulation of lysyl oxidase in spontaneous revertants of H-ras-transformed rat fibroblasts. Cancer Res 53:4670–4675PubMedGoogle Scholar
  57. Hamalainen ER, Jones TA, Sheer D, Taskinen K, Pihlajaniemi T, Kivirikko KI (1991) Molecular cloning of human lysyl oxidase and assignment of the gene to chromosome 5q23.3–31.2. Genomics 11:508–516PubMedCrossRefGoogle Scholar
  58. Hamalainen ER, Kemppainen R, Pihlajaniemi T, Kivirikko KI (1993) Structure of the human lysyl oxidase gene. Genomics 17:544–548PubMedCrossRefGoogle Scholar
  59. Hämäläinen ER, Kemppainen R, Kuivaniemi H, Tromp G, Vaheri A, Pihlajaniemi T, Kivirikko KI (1995) Quantitative polymerase chain reaction of lysyl oxidase mRNA in malignantly transformed human cell lines demonstrates that their low lysyl oxidase activity is due to low quantities of its mRNA and low levels of transcription of the respective gene. J Biol Chem 270(37):21590–21593PubMedGoogle Scholar
  60. Harlow CR, Rae M, Davidson L, Trackman PC, Hillier SG (2003) Lysyl oxidase gene expression and enzyme activity in the rat ovary: regulation by follicle-stimulating hormone, androgen, and transforming growth factor-beta superfamily members in vitro. Endocrinology 144:154–162PubMedCrossRefGoogle Scholar
  61. Hasebe T, Mukai K, Tsuda H, Ochiai A (2000) New prognostic histological parameter of invasive ductal carcinoma of the breast: clinicopathological significance of fibrotic focus. Pathol Int 50:263–272PubMedCrossRefGoogle Scholar
  62. He J, Tang HJ, Wang YY, Xiong MH, Zhou F, Shao K, Li TP (2002) Expression of lysyl oxidase gene in upper digestive tract carcinomas and its clinical significance. Ai Zheng 21(6):671–674PubMedGoogle Scholar
  63. Hong HH, Trackman PC (2002) Cytokine regulation of gingival fibroblast lysyl oxidase, collagen, and elastin. J Periodontol 73:145–152PubMedCrossRefGoogle Scholar
  64. Hong HH, Uzel MI, Duan C, Sheff MC, Trackman PC (1999) Regulation of lysyl oxidase, collagen, and connective tissue growth factor by TGF-beta1 and detection in human gingival. Lab Invest 79:1655–1667PubMedGoogle Scholar
  65. Huang Y, Dai J, Tang R, Zhao W, Zhou Z, Wang W, Ying K, Xie Y, Mao Y (2001) Cloning and characterization of a human lysyl oxidase-like 3 gene (hLOXL3). Matrix Biol 20:153–157PubMedCrossRefGoogle Scholar
  66. Hynes RO (2002) A reevaluation of integrins as regulators of angiogenesis. Nat Med 8:918–921PubMedCrossRefGoogle Scholar
  67. Jansen MK, Csiszar K (2007) Intracellular localization of the matrix enzyme lysyl oxidase in polarized epithelial cells. Matrix Biol 26:136–139PubMedCrossRefGoogle Scholar
  68. Jeay S, Pianetti S, Kagan HM, Sonenshein GE (2003) Lysyl oxidase inhibits ras-mediated transformation by preventing activation of NF-Kb. Mol Cell Biol 23:2251–2263PubMedCrossRefGoogle Scholar
  69. Jourdan-Le Saux C, Gleyzal C, Garnier JM, Peraldi M, Sommer P, Grimaud JA (1994) Lysyl oxidase cDNA of myofibroblast from mouse fibrotic liver. Biochem Biophys Res Commun 199:587–592PubMedCrossRefGoogle Scholar
  70. Jourdan-Le Saux C, Tronecker H, Bogic L, Bryant-Greenwood GD, Boyd CD, Csiszar K (1999) The LOXL2 gene encodes a new lysyl oxidase-like protein and is expressed at high levels in reproductive tissues. J. Biol. Chem 274:12939–12944PubMedCrossRefGoogle Scholar
  71. Juliano RL (2002) Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 42:283–323PubMedCrossRefGoogle Scholar
  72. Kagan HM (1986) Characterization and regulation of lysyl oxidase. In: Mecham RP (ed) Biology of extracellular matrix. Academic Press, Orlando, pp 321–389Google Scholar
  73. Kagan HM (1994) Lysyl oxidase: mechanism, regulation and relationship to liver fibrosis. Pathol Res Pract 190:910–919PubMedGoogle Scholar
  74. Kagan HM, Cai P (1995) Isolation of active site peptides of lysyl oxidase. Methods Enzymol 258:122–132PubMedCrossRefGoogle Scholar
  75. Kagan HM, Li W (2003) Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J Cell Biochem 88:660–672PubMedCrossRefGoogle Scholar
  76. Kagan HM, Raghavan J, Hollander W (1981) Changes in aortic lysyl oxidase activity in diet-induced atherosclerosis in the rabbit. Arteriosclerosis 1:287–291PubMedGoogle Scholar
  77. Kagan HM, Williams MA, Calaman SD, Berkowitz EM (1983) Histone H1 is a substrate for lysyl oxidase and contains endogenous sodium borotritide-reducible residues. Biochem Biophys Res Commun 115:186–192PubMedCrossRefGoogle Scholar
  78. Kagan HM, Williams MA, Williamson PR, Anderson JM (1984) Influence of sequence and charge on the specificity of lysyl oxidase toward protein and synthetic peptide substrates. J Biol Chem 259:11203–11207PubMedGoogle Scholar
  79. Kaneda A, Wakazono K, Tsukamoto T, Watanabe N, Yagi Y, Tatematsu M, Kaminishi M, Sugimura T, Ushijima T (2004a) Lysyl oxidase is a tumor suppressor gene inactivated by methylation and loss of heterozygosity in human gastric cancers. Cancer Res 64:6410–6415PubMedCrossRefGoogle Scholar
  80. Kaneda A, Wakazono K, Tsukamoto T, Watanabe N, Yagi Y, Tatematsu M, Kaminishi M, Sugimura T, Ushijima T (2004b) Lysyl oxidase is a tumor suppressor gene inactivated by methylation and loss of heterozygosity in human gastric cancers. Cancer Res 64(18):6410–6415PubMedCrossRefGoogle Scholar
  81. Kannan K, Amariglio N, Rechavi G, Jakob-Hirsch J, Kela I, Kaminski N, Getz G, Domany E, Givol D (2001) DNA microarrays identification of primary and secondary target genes regulated by p53. Oncogene 20:2225–2234PubMedCrossRefGoogle Scholar
  82. Kenyon K, Contente S, Trackman PC, Tang J, Kagan HM, Friedman RM (1991) Lysyl oxidase and rrg messenger RNA. Science 253:802PubMedCrossRefGoogle Scholar
  83. Kenyon K, Modi WS, Contente S, Friedman RM (1993) A novel human cDNA with a predicted protein similar to lysyl oxidase maps to chromosome 15q24–q25. J Biol Chem 268:18435–18437PubMedGoogle Scholar
  84. Kessler E, Takahara K, Biniaminov L, Brusel M, Greenspan DS (1996) Bone morphogenetic protein-1: the type I procollagen C-proteinase. Science 271:360–362PubMedCrossRefGoogle Scholar
  85. Khakoo A, Thomas R, Trompeter R, Duffy P, Price R, Pope FM (1997) Congenital cutis laxa and lysyl oxidase deficiency. Clin Genet 51:109–114PubMedCrossRefGoogle Scholar
  86. Kim Y, Boyd CD, Csiszar K (1995) A new gene with sequence and structural similarity to the gene encoding human lysyl oxidase. J Biol Chem 270:7176–7182PubMedCrossRefGoogle Scholar
  87. Kirschmann DA, Seftor EA, Fong SF, Nieva DR, Sullivan CM, Edwards EM, Sommer P, Csiszar K, Hendrix MJ (2002) A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res 62:4478–4483PubMedGoogle Scholar
  88. Koch M, Foley JE, Hahn R, Zhou P, Burgeson RE, Gerecke DR, Gordon MK (2001) alpha 1(Xx) collagen, a new member of the collagen subfamily, fibril-associated collagens with interrupted triple helices. J Biol Chem 276:23120–23126PubMedCrossRefGoogle Scholar
  89. Korenaga Y, Matsuyama H, Hirata H, Nagao K, Ohmi C, Sakano S, Yoshihiro S, Naito K (2005) Smoking may cause genetic alterations at 5q22.2 approximately q23.1 in clear-cell renal cell carcinoma. Cancer Genet Cytogenet 163(1):7–11PubMedCrossRefGoogle Scholar
  90. Koslowski R, Seidel D, Kuhlisch E, Knoch KP (2003) Evidence for the involvement of TGF-beta and PDGF in the regulation of prolyl 4-hydroxylase and lysyloxidase in cultured rat lung fibroblasts. Exp Toxicol Pathol 55:257–264PubMedCrossRefGoogle Scholar
  91. Kosonen T, Uriu-Hare JY, Clegg MS, Keen CL, Rucker RB (1997) Incorporation of copper into lysyl oxidase. Biochem J 327:283–289PubMedGoogle Scholar
  92. Krzyzosiak WJ, Shindo-Okada N, Teshima H, Nakajima K, Nishimura S (1992) Isolation of genes specifically expressed in flat revertant cells derived from activated ras-transformed NIH 3T3 cells by treatment with azatyrosine. Proc Natl Acad Sci 89:4879–4883PubMedCrossRefGoogle Scholar
  93. Kuivaniemi H, Savolainen ER, Kivirikko KI (1984) Human placental lysyl oxidase. Purification, partial characterization, and preparation of two specific antisera to the enzyme. J Biol Chem 259:6996–7002PubMedGoogle Scholar
  94. Kuivaniemi H, Peltonen L, Kivirikko KI (1985) Type IX Ehlers–Danlos syndrome and Menkes syndrome: the decrease in lysyl oxidase activity is associated with a corresponding deficiency in the enzyme protein. Am J Hum Genet 37:798–808PubMedGoogle Scholar
  95. Kuivaniemi H, Ala-Kokko L, Kivirikko KI (1986a) Secretion of lysyl oxidase by cultured human skin fibroblasts and effects of monensin, nigericin, tunicamycin and colchicines. Biochim Biophys Acta 883:326–334PubMedGoogle Scholar
  96. Kuivaniemi H, Korhonen RM, Vaheri A, Kivirikko KI (1986b) Deficient production of lysyl oxidase in cultures of malignantly transformed human cells. FEBS Lett 195:261–264PubMedCrossRefGoogle Scholar
  97. Lapointe J, Li C, Higgins JP, van de Rijn M, Bair E, Montgomery K, Ferrari M, Egevad L, Rayford W, Bergerheim U, Ekman P, DeMarzo AM, Tibshirani R, Botstein D, Brown PO, Brooks JD, Pollack JR (2004) Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc Natl Acad Sci 101:811–816PubMedCrossRefGoogle Scholar
  98. Layman DL, Narayanan AS, Martin GR (1972) The production of lysyl oxidase by human fibroblasts in culture. Arch Biochem Biophys 149:97–101PubMedCrossRefGoogle Scholar
  99. Lazarus HM, Cruikshank WW, Narasimhan N, Kagan HM, Center DM (1994) Induction of human monocyte motility by lysyl oxidase. Mat Biol 14:727–731CrossRefGoogle Scholar
  100. Le QT, Kong C, Lavori PW, O’byrne K, Erler JT, Huang X, Chen Y, Cao H, Tibshirani R, Denko N, Giaccia AJ, Koong AC (2007) Expression and prognostic significance of a panel of tissue hypoxia markers in head-and-neck squamous cell carcinomas. Int J Radiat Oncol Biol Phys 69(1):167–175PubMedGoogle Scholar
  101. Li W, Nellaiappan K, Strassmaier T, Graham L, Thomas KM, Kagan HM (1997) Localization and activity of lysyl oxidase within nuclei of fibrogenic cells. Proc Natl Acad Sci 94:12817–12822PubMedCrossRefGoogle Scholar
  102. Li W, Liu G, Chou IN, Kagan HM (2000) Hydrogen peroxide-mediated, lysyl oxidase-dependent chemotaxis of vascular smooth muscle cells. J Cell Biol 78:550–557Google Scholar
  103. Li W, Nugent MA, Zhao Y, Chau AN, Li SJ, Chou IN, Liu G, Kagan HM (2003) Lysyl oxidase oxidizes basic fibroblast growth factor and inactivates its mitogenic potential. J Cell Biochem 88:152–164PubMedCrossRefGoogle Scholar
  104. Light ND, Bailey AJ (1980) The chemistry of the collagen cross-links. Purification and characterization of cross-linked polymeric peptide material from mature collagen containing unknown amino acids. Biochem J 185:373–381PubMedGoogle Scholar
  105. Lucero HA, Kagan HM (2006) Lysyl oxidase: an oxidative enzyme and effector of cell function. Cell Mol Life Sci 63:2304–2316PubMedCrossRefGoogle Scholar
  106. Maki JM, Tikkanen H, Kivirikko KI (2001) Cloning and characterization of a fifth human lysyl oxidase isoenzyme: the third member of the lysyl oxidase-related subfamily with four scavenger receptor cysteine-rich domains. Matrix Biol 20:493–496PubMedCrossRefGoogle Scholar
  107. Mariani TJ, Trackman PC, Kagan HM, Eddy RL, Shows TB, Bo yd CD (1992) The complete derived amino acid sequence of human lysyl oxidase and assignment of the gene to chromosome 5 (extensive sequence homology with the murine ras recision gene). Matrix 12:242–248PubMedGoogle Scholar
  108. Mello MLS, Contente S, Vidal BC, Planding W, Schenck U (1995) Modulation of ras transformation affecting chromatin supraorganization as assessed by image analysis. Exp Cell Res 22:374–382CrossRefGoogle Scholar
  109. Mock BA, Contente S, Kenyon K, Friedman RM, Kozak CA (1992) The gene for lysyl oxidase maps to mouse chromosome 18. Genomics 14:822–823PubMedCrossRefGoogle Scholar
  110. Myllyharju J, Kivirikko KI (2001) Collagens and collagen-related diseases. Ann Med 33:7–21PubMedCrossRefGoogle Scholar
  111. Nagan N, Kagan HM (1994) Modulation of lysyl oxidase activity toward peptidyl lysine by vicinal dicarboxylic amino acid residues. Implications for collagen cross-linking. J Biol Chem 269:22366–22371PubMedGoogle Scholar
  112. Nellaiappan K, Risitano A, Liu G, Nicklas G, Kagan HM (2000) Fully processed lysyl oxidase catalyst translocates from the extracellular space into nuclei of aortic smoothmuscle cells. J Cell Biochem 79:576–582PubMedCrossRefGoogle Scholar
  113. Nelson JM, Diegelmann RF, Cohen IK (1988) Effect of β-aminopropionitrile and ascorbate on fibroblast migration. Proc Soc Exp Biol Med 188:346–352PubMedGoogle Scholar
  114. Nishimura R, Hasebe T, Tsubono Y, Ono M, Sugitoh M, Arai T, Mukai K (1998) The fibrotic focus in advanced colorectal carcinoma: a hitherto unrecognized histological predictor for liver metastasis. Virchows Arch 433:517–522PubMedCrossRefGoogle Scholar
  115. Oganesian A, Au S, Horst JA, Holzhausen LC, Macy AJ, Pace JM (2006) The NH2-terminal propeptide of type I procollagen acts intracellularly to modulate cell function. J Biol Chem 281:38507–38518PubMedCrossRefGoogle Scholar
  116. Ohkawa K, Fujii K, Nishida A, Yamauchi T, Ishibashi H, Yamamoto H (2001) Lysyl oxidase-catalyzed cross-linking and insolubilization reactions of Lys-containing polypeptides and synthetic adhesive proteins. Biomacromolecules 2:773–779PubMedCrossRefGoogle Scholar
  117. Omori K, Fujiseki Y, Suzukawa J, Inagaki C (2002) Regulation of the expression of lysyl oxidase mRNA in cultured rabbit retinal pigment epithelium cells. Matrix Biol 21:337–348PubMedCrossRefGoogle Scholar
  118. Ooshima A, Midorikawa O (1977) Increased lysyl oxidase activity in blood vessels of hypertensive rats and effect of β-aminopropionitrile on arteriosclerosis. Jpn Circ J 41:1337–1340PubMedGoogle Scholar
  119. Opsahl W, Zeronian H, Ellison M, Lewis D, Rucker RB, Riggins RS (1982) Role of copper in collagen cross-linking and its influence on selected mechanical properties of chick bone and tendon. J Nutr 112:708–716PubMedGoogle Scholar
  120. Palamakumbura AH, Jeay S, Guo Y, Pischon N, Sommer P, Sonenshein GE, Trackman PC (2004) The propeptide domain of lysyl oxidase induces phenotypic reversion of ras-transformed cells. J Biol Chem 279:40593–40600PubMedCrossRefGoogle Scholar
  121. Panchenko MV, Stetler-Stevenson WG, Trubetskoy OV, Gacheru SN, Kagan HM (1996) Metalloproteinase activity secreted by fibrogenic cells in the processing of prolysyl oxidase. Potential role of procollagen C-proteinase. J Biol Chem 271:7113–7119PubMedCrossRefGoogle Scholar
  122. Paola AH, Siddharth V, Siddika Selva S, Dan Y, Cynthia St H, Ying G, Amitha HP, Barbara MS, Katya R, Philip CT (2008) Lysyl oxidase propeptide inhibits smooth muscle cell signaling and proliferation. Biochem Biophys Res Commun 366(1):156–161Google Scholar
  123. Payne SL, Hendrix MJ, Kirschmann DA (2007) Paradoxical roles for lysyl oxidases in cancer––a prospect. J Cell Biochem 101(6):1338–1354PubMedCrossRefGoogle Scholar
  124. Peltonen L, Kuivaniemi H, Palotie A, Horn N, Kaitila I, Kivirikko KI (1983) Alterations in copper and collagen metabolism in the Menkes syndrome and a new subtype of the Ehlers–Danlos syndrome. Biochemistry 22:6156–6163PubMedCrossRefGoogle Scholar
  125. Peyrol S, Raccurt M, Gerard F, Gleyzal C, Grimaud JA, Sommer P (1997) Lysyl oxidase gene expression in the stromal reaction to in situ and invasive ductal breast carcinoma. Am J Pathol 150:497–507PubMedGoogle Scholar
  126. Pinnell SR (1982) Molecular defects in the Ehlers–Danlos syndrome. J Invest Dermatol 79:90s–92sPubMedCrossRefGoogle Scholar
  127. Pinnell SR, Martin GR (1968) The cross-linking of collagen and elastin: enzymatic conversion of lysine in peptide linkage to -aminoadipic-delta-semialdehyde (allysine) by an extract from bone. Proc Natl Acad Sci 61:708–716PubMedCrossRefGoogle Scholar
  128. Polgar N, Fogelgren B, Shipley JM, Csiszar K (2007) Lysyl oxidase interact with hormone placental lactogen and synergistically promotes breast epithelial cell proliferation and migration. J Biol Chem 282:3262–3272PubMedCrossRefGoogle Scholar
  129. Prockop DJ, Sieron AL, Li SW (1998) Procollagen N-proteinase and procollagen C-proteinase. Two unusual metalloproteinases that are essential for procollagen processing probably have important roles in development and cell signaling. Matrix Biol 16:399–408PubMedCrossRefGoogle Scholar
  130. Reiser K, McCormick RJ, Rucker RB (1992) Enzymatic and nonenzymatic cross-linking of collagen and elastin. FASEB J 6:2439–2449PubMedGoogle Scholar
  131. Ren C, Yang G, Timme TL, Wheeler TM, Thompson TC (1998) Reduced lysyl oxidase messenger RNA levels in experimental and human prostate cancer. Cancer Res 58(6):1285–1290PubMedGoogle Scholar
  132. Romain D, Valérie C, Géraldine A, Valérie A, Martine D, Isabelle R, André M, Odile D, Pascal S (2010) Epigenetic silencing of lysyl oxidase-like-1 through DNA hypermethylation in an autosomal recessive cutis laxa case. J Invest Dermatol 130:2594–2601CrossRefGoogle Scholar
  133. Romero-Chapman N, Lee J, Tinker D, Uriu-Hare JY, Keen CL, Rucker RB (1990) Lysyl oxidase: purification, properties and influence of dietary copper on accumulation and functional activity in rat skin. Biochem J 275:657–662Google Scholar
  134. Ross DT, Scherf U, Eisen MB, Perou CM, Rees C, Spellman P, Iyer V, Jeffrey SS, Van de Rijn M, Waltham M, Pergamenschikov A, Lee JC, Lashkari D, Shalon D, Myers TG, Weinstein JN, Botstein D, Brown PO (2000) Systematic variation in gene expression patterns in human cancer cell lines. Nat Genet 24(3):227–235PubMedCrossRefGoogle Scholar
  135. Rost T, Pyritz V, Rathcke IO, Gorogh T, Dunne AA, Werner JA (2003) Reduction of LOX- and LOXL2-mRNA expression in head and neck squamous cell carcinomas. Anticancer Res 23(2B):1565–1573PubMedGoogle Scholar
  136. Roy R, Polgar P, Wang Y, Goldstein RH, Taylor L, Kagan HM (1996) Regulation of lysyl oxidase and cyclooxygenase expression in human lung fibroblasts: interactions among TGF-beta, IL-1 beta, and prostaglandin E. J Cell Biochem 62:411–417PubMedCrossRefGoogle Scholar
  137. Royce PM, Camakaris J, Danks DM (1980) Reduced lysyl oxidase activity in skin fibroblasts from patients with Menkes’ syndrome. Biochem J 192:579–586PubMedGoogle Scholar
  138. Rucker RB, Romero-Chapman N, Wong T, Lee J, Steinberg FM, Mcgee C, Clegg MS, Reiser K, Kosonen T, Uriu-Hare JY, Murphy J, Keen CL (1996) Modulation of lysyl oxidase by dietary copper in rats. J Nutr 126:51–60PubMedGoogle Scholar
  139. Rucker RB, Kosonen T, Clegg MS, Mitchell AE, Rucker BR, Uriu-Hare JY, Keen CL (1998) Copper, lysyl oxidase, and extracellular matrix protein cross-linking. Am J Clin Nutr 67:996–1002Google Scholar
  140. Saito H, Papaconstantinou J, Sato H, Goldstein S (1997) Regulation of a novel gene encoding a lysyl oxidase-related protein in cellular adhesion and senescence. J Biol Chem 272:8157–8160PubMedCrossRefGoogle Scholar
  141. Sanada H, Shikata J, Hamamoto H, Ueba Y, Yamamuro T, Takeda T (1978) Changes in collagen cross-linking and lysyl oxidase by estrogen. Biochim Biophys Acta 541:408–413PubMedGoogle Scholar
  142. Sawada S, Murakami K, Murata J, Tsukada K, Saiki I (2001) Accumulation of extracellular matrix in the liver induces high metastatic potential of hepatocellular carcinoma to the lung. Int J Oncol 19:65–70PubMedGoogle Scholar
  143. Schuppan D, Ruehl M, Somasundaram R, Hahn EG (2001) Matrix as a modulator of hepatic fibrogenesis. Semin Liver Dis 21:351–372PubMedCrossRefGoogle Scholar
  144. Shackleton DR, Hulmes DJ (1990) Purification of lysyl oxidase from piglet skin by selective interaction with Sephacryl S-200. Biochem J 266:917–919PubMedGoogle Scholar
  145. Shames DS, Girard L, Gao B, Sato M, Lewis CM, Shivapurkar N, Jiang A, Perou CM, Kim YH, Pollack JR, Fong KM, Lam CL, Wong M, Shyr Y, Nanda R, Olopade OI, Gerald W, Euhus DM, Shay JW, Gazdar AF, Minna JD (2006) A genome-wide screen for promoter methylation in lung cancer identifies novel methylation markers for multiple malignancies. PLoS Med 3(12):e486PubMedCrossRefGoogle Scholar
  146. Shanley CJ, Gharaee-Kermani M, Sarkar R, Welling TH, Kriegel A, Ford JW, Stanley JC, Phan SH (1997) Transforming growth factor-beta 1 increases lysyl oxidase enzyme activity and mRNA in rat aortic smooth muscle cells. J Vasc Surg 25:446–452PubMedCrossRefGoogle Scholar
  147. Shibanuma M, Mashimo J, Mita A, Kuroki T, Nose K (1993) Cloning from a mouse osteoblastic cell line of a set of transforming-growth-factor-beta 1-regulated genes, one of which seems to encode a follistatin-related polypeptide. Eur J Biochem 217:13–19PubMedCrossRefGoogle Scholar
  148. Siegel RC (1974) Biosynthesis of collagen crosslinks: increased activity of purified lysyl oxidase with reconstituted collagen fibrils. Proc Natl Acad Sci 71:4826–4830PubMedCrossRefGoogle Scholar
  149. Slee RB, Hillier SG, Largue P, Harlow CR, Miele G, Clinton M (2001) Differentiation-dependent expression of connective tissue growth factor and lysyl oxidase messenger ribonucleic acids in rat granulosa cells. Endocrinology 142:1082–1089PubMedCrossRefGoogle Scholar
  150. Smith-Mungo LI, Kagan HM (1998) Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol 16:387–398PubMedCrossRefGoogle Scholar
  151. Smith-Mungo LI, Kagan HM (2002) PKC-MEK-MAPK-dependent signal transduction pathway mediates the stimulation of lysyl oxidase expression by serum and PDGF in rat aortic smooth muscle cells. J Cell Biochem 85:775–784PubMedCrossRefGoogle Scholar
  152. Sommer P, Gleyzal C, Raccurt M, Delbourg M, Serrar M, Joazeiro P, Peyrol S, Kagan HM, Trackman PC, Grimaud JA (1993) Transient expression of lysyl oxidase by liver myofibroblasts in murine schistosomiasis. Lab Invest 69:460–470PubMedGoogle Scholar
  153. Song YL, Ford JW, Gordon D, Shanley CJ (2000) Regulation of lysyl oxidase by interferon-gamma in rat aortic smooth muscle cells. Arterioscler Thromb Vasc Biol 20:982–988PubMedGoogle Scholar
  154. Stamenkovic I (2000) Matrix metalloproteinases in tumor invasion and metastasis. Semin Cancer Biol 10:415–433PubMedCrossRefGoogle Scholar
  155. Stassar MJ, Devitt G, Brosius M, Rinnab L, Prang J, Schradin T, Simon J, Petersen S, Kopp-Schneider A, Zoller M (2001) Identification of human renal cell carcinoma associated genes by suppression subtractive hybridization. Br J Cancer 85:1372–1382PubMedCrossRefGoogle Scholar
  156. Stassen FL (1976) Properties of highly purified lysyl oxidase from embryonic chick cartilage. Biochim Biophys Acta 438:49–60PubMedGoogle Scholar
  157. Stewart GD, Nanda J, Brown DJ, Riddick AC, Ross JA, Habib FK (2009) NO-sulindac inhibits the hypoxia response of PC-3 prostate cancer cells via the Akt signalling pathway. Int J Cancer 124(1):223–232PubMedCrossRefGoogle Scholar
  158. Takahara K, Lyons GE, Greenspan DS (1994) Bone morphogenetic protein-1 and a mammalian tolloid homologue (mTld) are encoded by alternatively spliced transcripts which are differentially expressed in some tissues. J Biol Chem 269:32572–32578PubMedGoogle Scholar
  159. Tan RS, Taniguchi T, Harada H (1996) Identification of the lysyl oxidase gene as target of the antioncogenic transcription factor, IRF-1, and its possible role in tumor suppression. Cancer Res 56:2417–2421PubMedGoogle Scholar
  160. Trackman PC, Pratt AM, Wolanski A, Tang SS, Offner GD, Troxler RF, Kagan HM (1990) Cloning of rat aorta lysyl oxidase cDNA: complete codons and predicted amino acid sequence. Biochemistry 29:4863–4870PubMedCrossRefGoogle Scholar
  161. Trackman PC, Pratt AM, Wolanski A, Tang SS, Offner GD, Troxler RF, Kagan HM (1991) Cloning of rat aorta lysyl oxidase cDNA: complete codons and predicted amino acid sequence. Biochemistry 30:8282PubMedCrossRefGoogle Scholar
  162. Trackman PC, Bedell-Hogan D, Tang J, Kagan HM (1992) Post-translational glycosylation and proteolytic processing of a lysyl oxidase precursor. J Biol Chem 267:8666–8671PubMedGoogle Scholar
  163. Trackman PC, Graham RJ, Bittner HK, Carnes DL, Gilles JA, Graves DT (1998) Inflammation-associated lysyl oxidase protein expression in vivo, and modulation by FGF-2 plus IGF-1. Histochem Cell Biol 110:9–14PubMedCrossRefGoogle Scholar
  164. Tsuchiya MI, Okuda H, Takaki Y, Baba M, Hirai SI, Ohno S, Shuin T (2005) Renal cell carcinoma- and pheochro-mocytoma-specific altered gene expression profiles in VHL mutant clones. Oncol Rep 13:1033–1041PubMedGoogle Scholar
  165. Urashima T, Zhao M, Wagner R, Fajardo G, Farahani S, Quertermous T, Bernstein D (2008) Molecular and physiological characterization of RV remodeling in a murine model of pulmonary stenosis. Am J Physiol Heart Circ Physiol 295(3):H1351–H1368PubMedCrossRefGoogle Scholar
  166. Uzel MI, Shih SD, Gross H, Kessler E, Gerstenfeld LC, Trackman PC (2000) Molecular events that contribute to lysyl oxidase enzyme activity and insoluble collagen accumulation in osteosarcoma cell clones. J Bone Miner Res 15:1189–1197PubMedCrossRefGoogle Scholar
  167. Uzel MI, Scott IC, Babakhanlou-Chase H, Palamakumbura AH, Pappano WN, Hong HH, Greenspan DS, Trackman PC (2001) Multiple bone morphogenetic protein 1-related mammalian metalloproteinases process pro-lysyl oxidase at the correct physiological site and control lysyl oxidase activation in mouse embryo fibroblast cultures. J Biol Chem 276:22537–22543PubMedCrossRefGoogle Scholar
  168. Vlodavsky I, Friedmann Y (2001) Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J Clin Invest 108:341–347PubMedGoogle Scholar
  169. Vrhovski B, Weiss AS (1998) Biochemistry of tropoelastin. Eur J Biochem 258:1–18PubMedCrossRefGoogle Scholar
  170. Wakasaki H, Ooshima A (1990) Immunohistochemical localization of lysyl oxidase with monoclonal antibodies. Lab Invest 63:377–384PubMedGoogle Scholar
  171. Watanabe T, Ichihara M, Hashimoto M, Shimono K, Shimoyama Y, Nagasaka T, Murakumo Y, Murakami H, Sugiura H, Iwata H, Ishiguro N, Takahashi M (2002) Characterization of gene expression induced by RET with MEN2A or MEN2B mutation. Am J Pathol 161(1):249–256PubMedGoogle Scholar
  172. Wolf C (2010) Lysyl oxidase-like 1 gene polymorphisms in german patients with normal tension glaucoma, pigmentary glaucoma and exfoliation glaucoma. J Glaucoma 19(2):136–141PubMedGoogle Scholar
  173. Wu Y, Rich CB, Lincecum J, Trackman PC, Kagan HM, Foster JA (1992) Characterization and developmental expression of chick aortic lysyl oxidase. J Biol Chem 267:24199–24206PubMedGoogle Scholar
  174. Wu M, Min C, Wang X, Yu Z, Kirsch KH, Trackman PC, Sonenshein GE (2007) Repression of BCL2 by the tumor suppressor activity of the lysyl oxidase propeptide inhibits transformed phenotype of lung and pancreatic cancer cells. Cancer Res 67(13):6278–6285PubMedCrossRefGoogle Scholar
  175. Yeowell HN, Marshall MK, Walker LC, Ha V, Pinnell SR (1994) Regulation of lysyl oxidase mRNA in dermal fibroblasts from normal donors and patients with inherited connective tissue disorders. Arch Biochem Biophys 308:299–305PubMedCrossRefGoogle Scholar
  176. Zhou Y, Wang X, Jiang L, Tan R, Xiong M, He W, Fang Li, Wen P, Yang J (2010) Uric acid increases fibronectin synthesis through upregulation of lysyl oxidase expression in rat renal tubular epithelial cells. Am J Physiol Renal Physiol 299:F336–F346CrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2010

Authors and Affiliations

  • Siddikuzzaman
    • 1
  • V. M. Berlin Grace
    • 1
  • C. Guruvayoorappan
    • 1
  1. 1.Department of BiotechnologyKarunya UniversityCoimbatoreIndia

Personalised recommendations