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Review Article

LOX/LOXL in pulmonary fibrosis: potential therapeutic targets

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Pages 790-796 | Received 12 Sep 2018, Accepted 12 Nov 2018, Published online: 29 Nov 2018

References

  • Kagan HM. Characterization and regulation of lysyl oxidase. In Mecham RP ed. Biology of extracellular matrix. Orlando: Academic Press; 1986. p 321–389.
  • Kenyon K, Modi WS, Contente S, et al. A novel human cDNA with a predicted protein similar to lysyl oxidase maps to chromosome 15q24-q25. J Biol Chem. 1993;268:18435–18437.
  • Kim Y, Boyd CD, Csiszar K. A new gene with sequence and structural similarity to the gene encoding human lysyl oxidase. J Biol Chem. 1995;270:7176–7182.
  • Saito H, Papaconstantinou J, Sato H, et al. Regulation of a novel gene encoding a lysyl oxidase-related protein in cellular adhesion and senescence. J Biol Chem. 1997;272:8157–8160.
  • Jourdan-Le Saux C, Tronecker H, Bogic L, et al. The LOXL2 gene encodes a new lysyl oxidase-like protein and is expressed at high levels in reproductive tissues. J Biol Chem. 1999;274:12939–12944.
  • Maki JM, Kivirikko KI. Cloning and characterization of a fourth human lysyl oxidase isoenzyme. Biochem J. 2001;355:381–387.
  • Huang Y, Dai J, Tang R, et al. Cloning and characterization of a human lysyl oxidase-like 3 gene (hLOXL3). Matrix Biol. 2001;20:153–157.
  • Asuncion L, Fogelgren B, Fong KS, et al. A novel human lysyl oxidase-like gene (LOXL4) on chromosome 10q24 has an altered scavenger receptor cysteine rich domain. Matrix Biol. 2001;20:487–491.
  • Maki JM, Tikkanen H, Kivirikko KI. 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. 2001;20:493–496.
  • Csiszar K. Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol. 2001;70:1–32.
  • Barker HE, Cox TR, Erler JT. The rationale for targeting the LOX family in cancer. Nat Rev Cancer. 2012;12:540–552.
  • Trackman PC. Lysyl oxidase isoforms and potential therapeutic opportunities for fibrosis and cancer. Exp Opin Ther Targets. 2016;20:935–945.
  • Trackman PC, Bedell-Hogan D, Tang J, et al. Post-translational glycosylation and proteolytic processing of a lysyl oxidase precursor. J Biol Chem. 1992;267:8666–8671.
  • Uzel MI, Shih SD, Gross H, et al. Molecular events that contribute to lysyl oxidase enzyme activity and insoluble collagen accumulation in osteosarcoma cell clones. J Bone Miner Res. 2000;15:1189–1197.
  • Kagan HM, Li W. Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J Cell Biochem. 2003;88:660–672.
  • Siegel RC, Chen KH, Greenspan JS, et al. Biochemical and immunochemical study of lysyl oxidase in experimental hepatic fibrosis in the rat. Proc Natl Acad Sci USA. 1978;75:2945–2949.
  • Carter EA, McCarron MJ, Alpert E, et al. Lysyl oxidase and collagenase in experimental acute and chronic liver injury. Gastroenterology. 1982;82:526–534.
  • Wakasaki H, Ooshima A. Synthesis of lysyl oxidase in experimental hepatic fibrosis. Biochem Biophys Res Commun. 1990;166:1201–1204.
  • Murawaki Y, Kusakabe Y, Hirayama C. Serum lysyl oxidase activity in chronic liver disease in comparison with serum levels of prolyl hydroxylase and laminin. Hepatology. 1991;14:1167–1173.
  • Liu SB, Ikenaga N, Peng ZW, et al. Lysyl oxidase activity contributes to collagen stabilization during liver fibrosis progression and limits spontaneous fibrosis reversal in mice. Faseb J. 2016;30:1599–1609.
  • Counts DF, Evans JN, Dipetrillo TA, et al. Collagen lysyl oxidase activity in the lung increases during bleomycin-induced lung fibrosis. J Pharmacol Exp Ther. 1981;219:675–678.
  • Almassian B, Trackman PC, Iguchi H, et al. Induction of lung lysyl oxidase activity and lysyl oxidase protein by exposure of rats to cadmium chloride: properties of the induced enzyme. Connect Tissue Res. 1991;25:197–208.
  • Cheng T, Liu Q, Zhang R, et al. Lysyl oxidase promotes bleomycin-induced lung fibrosis through modulating inflammation. J Mol Cell Biol. 2014;6:506–515.
  • Lu J, Qian Y, Jin W, et al. Hypoxia-inducible factor-1α regulates epithelial-to-mesenchymal transition in paraquat-induced pulmonary fibrosis by activating lysyl oxidase. Exp Ther Med. 2018;15:2287–2294.
  • Goto Y, Uchio-Yamada K, Anan S, et al. Transforming growth factor-beta1 mediated up-regulation of lysyl oxidase in the kidneys of hereditary nephrotic mouse with chronic renal fibrosis. Virchows Arch. 2005;447:859–868.
  • Kagan HM, Raghavan J, Hollander W. Changes in aortic lysyl oxidase activity in diet-induced atherosclerosis in the rabbit. Arteriosclerosis. 1981;1:287–291.
  • Ovchinnikova OA, Folkersen L, Persson J, et al. The collagen cross-linking enzyme lysyl oxidase is associated with the healing of human atherosclerotic lesions. J Intern Med. 2014;276:525–536.
  • Vulpe C, Levinson B, Whitney S, et al. Isolation of a candidate gene for menkes disease and evidence that it encodes a copper-transporting ATPase. Nat Genet. 1993;3:7–13.
  • Chou DK, Zhao Y, Gao S, et al. Perturbation of copper (Cu) homeostasis and expression of Cu-binding proteins in cadmium-resistant lung fibroblasts. Toxicol Sci. 2007;99:267–276.
  • Kim D, Choi J, Han KM, et al. Impaired osteogenesis in Menkes disease-derived induced pluripotent stem cells. Stem Cell Res Ther. 2015;6:160–171.
  • Sasaki T, Stoop R, Sakai T, et al. Loss of fibulin-4 results in abnormal collagen fibril assembly in bone, caused by impaired lysyl oxidase processing and collagen cross-linking. Matrix Biol. 2016;50:53–66.
  • Erler JT, Bennewith KL, Nicolau M, et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature. 2006;440:1222–1226.
  • Stassen FL. Properties of highly purified lysyl oxidase from embryonic chick cartilage. Biochim Biophys Acta. 1976;438:49–60.
  • Kagan HM, Sullivan KA, Olsson TA, et al. Purification and properties of four species of lysyl oxidase from bovine aorta. Biochem J. 1979;177:203–214.
  • Cronlund AL, Kagan HM. Comparison of lysyl oxidase from bovine lung and aorta. Connect Tissue Res. 1986;15:173–185.
  • Kuivaniemi H, Savolainen ER, Kivirikko KI. Human placental lysyl oxidase. Purification, partial characterization, and preparation of two specific antisera to the enzyme. J Biol Chem. 1984;259:6996–7002.
  • Shackleton DR, Hulmes DJ. Purification of lysyl oxidase from piglet skin by selective interaction with Sephacryl S-200. Biochem J. 1990;266:917–919.
  • Trackman PC, Pratt AM, Wolanski A, et al. Cloning of rat aorta lysyl oxidase cDNA: complete codons and predicted amino acid sequence. Biochemistry. 1990;29:4863–4870.
  • Trackman PC, Pratt AM, Wolanski A, et al. Cloning of rat aorta lysyl oxidase cDNA: complete codons and predicted amino acid sequence. Biochemistry. 1991;30:8282.
  • Contente S, Csiszar K, Kenyon K, et al. Structure of the mouse lysyl oxidase gene. Genomics. 1993;16:395–400.
  • Wu Y, Rich CB, Lincecum J, et al. Characterization and developmental expression of chick aortic lysyl oxidase. J Biol Chem. 1992;267:24199–24206.
  • Hamalainen ER, Jones TA, Sheer D, et al. Molecular cloning of human lysyl oxidase and assignment of the gene to chromosome 5q23.3-31.2. Genomics. 1991;11:508–516.
  • Hamalainen ER, kemppainen R, Pihlajaniemi T, et al. Structure of the human lysyl oxidase gene. Genomics. 1993;17:544–548.
  • Mariani TJ, Trackman PC, Kagan HM, et al. 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. 1992;12:242–248.
  • Boyd CD, Mariani TJ, Kim Y, et al. The size heterogeneity of human lysyl oxidase mRNA is due to alternate polyadenylation site and not alternate exon usage. Mol Biol Rep. 1995;21:95–103.
  • Fujimaki T, Hotta Y, Sakuma H, et al. Large-scale sequencing of the rabbit corneal endothelial cDNA library. Cornea. 1999;18:109–114.
  • Gregory KE, Marsden ME, Anderson-MacKenzie J, et al. Abnormal collagen assembly, though normal phenotype, in alginate bead cultures of chick embryo chondrocytes. Exp Cell Res. 1999;246:98–107.
  • Baccarani-Contri M, Vincenzi D, Quaglino D, Jr, et al. Localization of human placenta lysyl oxidase on human placenta, skin and aorta by immunoelectronmicroscopy. Matrix. 1990;9:428–436.
  • Kagan HM, Williams MA, Calaman SD, et al. Histone H1 is a substrate for lysyl oxidase and contains endogenous sodium borotritide-reducible residues. Biochem Biophys Res Commun. 1983;115:186–189.
  • Giampuzzi M, Oleggini R, Di Donato A. Demonstration of in vitro interaction between tumor suppressor lysyl oxidase and histones H1 and H2: definition of the regions involved. Biochim Biophys Acta. 2003;1647:245–251.
  • Li W, Nugent MA, Zhao Y, et al. Lysyl oxidase oxidizes basic fibroblast growth factor and inactivates its mitogenic potential. J Cell Biochem. 2003;88:152–164.
  • Nelson JM, Diegelmann RF, Cohen IK. Effect of beta-aminopropionitrile and ascorbate on fibroblast migration. Proc Soc Exp Biol Med. 1988;188:346–352.
  • Lazarus HM, Cruikshank WW, Narasimhan N, et al. Induction of human monocyte motility by lysyl oxidase. Matrix Biol. 1995;14:727–731.
  • Li W, Liu G, Chou IN, et al. Hydrogen peroxide-mediated, lysyl oxidase-dependent chemotaxis of vascular smooth muscle cells. J Cell Biochem. 2000;78:550–557.
  • Li W, Nellaiappan K, Strassmaier T, et al. Localization and activity of lysyl oxidase within nuclei of fibrogenic cells. Proc Natl Acad Sci USA. 1997;94:12817–12822.
  • Giampuzzi M, Botti G, Di Duca M, et al. Lysyl oxidase activates the transcription activity of human collagene III promoter. Possible involvement of Ku antigen. J Biol Chem. 2000;275:36341–36349.
  • Oleggini R, Gastaldo N, Di Donato A. Regulation of elastin promoter by lysyl oxidase and growth factors: cross control of lysyl oxidase on TGF-beta1 effects. Matrix Biol. 2007;26:494–505.
  • Mižíková I, Palumbo F, Tábi T, et al. Perturbations to lysyl oxidase expression broadly influence the transcriptome of lung fibroblasts. Physiol Genomics. 2017;49:416–429.
  • Bellaye PS, Shimbori C, Upagupta C, et al. Lysyl oxidase-like 1 protein deficiency protects mice from adenoviral transforming growth factor-β1-induced pulmonary fibrosis. Am J Respir Cell Mol Biol. 2018;58:461–470.
  • Du Bois RM. Strategies for treating idiopathic pulmonary fibrosis. Nat Rev Drug Discov. 2010;9:129–140.
  • Sgalla G, Iovene B, Calvello M, et al. Idiopathic pulmonary fibrosis: pathogenesis and management. Respir Res. 2018;19:32–50.
  • Lederer DJ, Martinez FJ. Idiopathic pulmonary fibrosis. N Engl J Med. 2018;378:1811–1823.
  • Dimitroulis IA. Nintedanib: a novel therapeutic approach for idiopathic pulmonary fibrosis. Respir Care. 2014;59:1450–1455.
  • Richeldi L, du Bois RM, Raghu G, et al. Efficacy and safety of nintedanib in idiopathic pulmonary fibrosis. N Engl J Med. 2014;370:2071–2082.
  • King TE, Jr, Bradford WZ, Castro-Bernardini S, et al. A phase 3 trial of pirfenidone in patients with idiopathic pulmonary fibrosis. N Engl J Med. 2014;370:2083–2092.
  • Costabel U, Inoue Y, Richeldi L, et al. Efficacy of nintedanib in idiopathic pulmonary fibrosis across prespecified subgroups in INPULSIS. Am J Respir Crit Care Med. 2016;193:178–185.
  • Ley B, Swigris J, Day BM, et al. Pirfenidone reduces respiratory-related hospitalizations in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2017;196:756–761.
  • Raghu G, Rochwerg B, Zhang Y, et al. An official ATS/ERS/JRS/ALAT clinical practice guideline: treatment of idiopathic pulmonary fibrosis. An update of the 2011 clinical practice guideline. Am J Respir Crit Care Med. 2015;192:e3–e19.
  • Raghu G, Richeldi L. Current approaches to the management of idiopathic pulmonary fibrosis. Respir Med. 2017;129:24–30.
  • Raghu G, Anstrom KJ, King TE, Jr, et al. Prednisone, azathioprine, and N-acetylcysteine for pulmonary fibrosis, Idiopathic Pulmonary Fibrosis Clinical Research Network. N Engl J Med. 2012;366:1968–1977.
  • Martinez FJ, de Andrade JA, Anstrom KJ, et al. Randomized trial of acetylcysteine in idiopathic pulmonary fibrosis. Idiopathic Pulmonary Fibrosis Clinical Research Network. N Engl J Med. 2014;370:2093–2101.
  • Oldham JM, Ma SF, Martinez FJ, et al. TOLLIP, MUC5B, and the Response to N-Acetylcysteine among Individuals with Idiopathic Pulmonary Fibrosis. Am J Respir Crit Care Med. 2015;192:1475–1482.
  • King TE, Jr, Albera C, Bradford WZ, et al. Effect of interferon gamma-1b on survival in patients with idiopathic pulmonary fibrosis (INSPIRE): a multicentre, randomised, placebo-controlled trial. Lancet. 2009;374:222–228.
  • Raghu G, Behr J, Brown KK, et al. Treatment of idiopathic pulmonary fibrosis with ambrisentan: a parallel, randomized trial. Ann Intern Med. 2013;158:641–649.
  • Noth I, Anstrom KJ, Calvert SB, et al. A placebo-controlled randomized trial of warfarin in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2012;186:88–95.
  • Kreuter M, Wuyts W, Renzoni E, et al. Antacid therapy and disease outcomes in idiopathic pulmonary fibrosis: a pooled analysis. Lancet Respir Med. 2016;4:381–389.
  • Chen LJ, Li WD, Li SF, et al. Bleomycin induces upregulation of lysyl oxidase in cultured human fetal lung fibroblasts. Acta Pharmacol Sin. 2010;31:554–559.
  • Li S, Yang X, Li W, et al. N-acetylcysteine downregulation of lysyl oxidase activity alleviating bleomycin-induced pulmonary fibrosis in rats. Respiration. 2012;84:509–517.
  • Demedts M, Behr J, Buhl R, et al. High-dose acetylcysteine in idiopathic pulmonary fibrosis. N Engl J Med. 2005;353:2229–2242.
  • Behr J, Bendstrup E, Crestani B, et al. Safety and tolerability of acetylcysteine and pirfenidone combination therapy in idiopathic pulmonary fibrosis: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Respir Med. 2016;4:445–453.
  • Behr J, Crestani B, Wells A, et al. N-acetylcysteine for idiopathic pulmonary fibrosis: the door is still open-Authors' reply. Lancet Respir Med. 2017;5:e3.
  • Raghu G, Noth I, Martinez F. N-acetylcysteine for idiopathic pulmonary fibrosis: the door is still open. Lancet Respir Med. 2017;5:e1–e2.
  • Wijsenbeek MS, Collard HR. Acetylcysteine in IPF: the knockout blow?. Lancet Respir Med. 2016;4:420–421.
  • Chen LJ, Zhao Y, Gao S, et al. Downregulation of lysyl oxidase and upregulation of cellular thiols in rat fetal lung fibroblasts treated with cigarette smoke condensate. Toxicol Sci. 2005;83:372–379.
  • Rucker RB, Romero-Chapman N, Wong T, et al. Modulation of lysyl oxidase by dietary copper in rats. J Nutr. 1996;126:51–60.
  • Zhao Y, Gao S, Chou IN, et al. Inhibition of the expression of lysyl oxidase and its substrates in cadmium-resistant rat fetal lung fibroblasts. Toxicol Sci. 2006;90:478–489.
  • Zhang HD, Chen HC, Shan LF. Study on the relationship between copper, lysyl oxidase and premature rupture of membranes. Zhonghua Fu Chan Ke Za Zhi. 2006;41:7–11.
  • Ovet H, Oztay F. The copper chelator tetrathiomolybdate regressed bleomycin-induced pulmonary fibrosis in mice, by reducing lysyl oxidase expressions. Biol Trace Elem Res. 2014;162:189–199.
  • Mattie MD, Freedman JH. Copper-inducible transcription: regulation by metal- and oxidative stress-responsive pathways. Am J Physiol Cell Physiol. 2004;286:C293–C301.
  • Gao S, Zhao Y, Kong L, et al. Cloning and characterization of the rat lysyl oxidase gene promoter: Identification of core promoter elements and functional nuclear factor I binding sites. J Biol Chem. 2007;282:25322–25337.
  • Tjin G, White ES, Faiz A, et al. Lysyl oxidases regulate fibrillar collagen remodelling in idiopathic pulmonary fibrosis. Dis Model Mech. 2017;10:1301–1312.
  • Aumiller V, Strobel B, Romeike M, et al. Comparative analysis of lysyl oxidase (like) family members in pulmonary fibrosis. Sci Rep. 2017;7:149.
  • Chien JW, Richards TJ, Gibson KF, et al. Serum lysyl oxidase-like 2 levels and idiopathic pulmonary fibrosis disease progression. Eur Respir J. 2014;43:1430–1438.
  • Barry-Hamilton V, Spangler R, Marshall D. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med. 2010;16:1009–1017.
  • Meyer KC. Great expectations for simtuzumab in IPF fall short. Lancet Respir Med. 2017;5:2–3. Comment
  • Cuevas EP, Moreno-Bueno G, Canesin G, et al. LOXL2 catalytically inactive mutants mediate epithelial-to-mesenchymal transition. Biol Open. 2014;3:129–137.
  • Raghu G, Brown KK, Collard HR, et al. Efficacy of simtuzumab versus placebo in patients with idiopathic pulmonary fibrosis: a randomised, double-blind, controlled, phase 2 trial. Lancet Respir Med. 2017;5:22–32.

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