Lysyl hydroxylase 2 induces a collagen cross-link switch in tumor stroma

Journal of Clinical Investigation

Volumn 125, Issue 3, 2015, Pages 1147-1162

  Chen, Yulong ^a   Terajima, Masahiko ^b   Yang, Yanan ^c   Sun, Li ^a   Ahn, Young Ho ^a,d   Pankova, Daniela ^a   Puperi, Daniel S ^e   Watanabe, Takeshi ^b   Kim, Min P ^f   Blackmon, Shanda H ^f   Rodriguez, Jaime ^a   Liu, Hui ^a   Behrens, Carmen ^a   Wistuba, Ignacio I ^a   Minelli, Rosalba ^g   Scott, Kenneth L ^g   Sanchez Adams, Johannah ^h   Guilak, Farshid ^h   Pati, Debananda ^g   Thilaganathan, Nishan ^a   Burns, Alan R ⁱ   Creighton, Chad J ^a,g   Martinez, Elisabeth D ^j,k   Zal, Tomasz ^a   Grande Allen, K Jane ^e   Yamauchi, Mitsuo ^b   Kurie, Jonathan M ^a   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c MAYO CLINIC CANCER CENTER   (United States)

^d Ewha Womans University School of Medicine   (South Korea)

^e Rice University   (United States)

^f HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^g BAYLOR COLLEGE OF MEDICINE   (United States)

^h DUKE UNIVERSITY MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF HOUSTON   (United States)

^j UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^k UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; HYDROXYLYSINE ALDEHYDE DERIVED COLLAGEN CROSS LINK; HYPOXIA INDUCIBLE FACTOR 1; JANUS KINASE INHIBITOR; K RAS PROTEIN; LYSINE ALDEHYDE DERIVED CROSS LINK; PROCOLLAGEN LYSINE 2 OXOGLUTARATE 5 DIOXYGENASE; PROTEIN P21; STAT3 PROTEIN; SURFACTANT PROTEIN C; UNCLASSIFIED DRUG; PLOD2 PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER PROGNOSIS; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; COLLAGEN CROSS LINK; CONNECTIVE TISSUE TUMOR; CONTROLLED STUDY; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY CANCER; LUNG ADENOCARCINOMA; LUNG CANCER; LUNG METASTASIS; LUNG PARENCHYMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CROSS LINKING; PROTEIN DEPLETION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; TRANSMISSION ELECTRON MICROSCOPY; TUMOR GROWTH; TUMOR STROMA; TUMOR VOLUME; UPREGULATION; 129 MOUSE; ADENOCARCINOMA; ANIMAL; CANCER TRANSPLANTATION; CELL CULTURE; ENZYME INDUCTION; ENZYMOLOGY; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION; KAPLAN MEIER METHOD; LUNG TUMOR; MALE; METABOLISM; MORTALITY; PATHOLOGY; PHYSIOLOGY; SECONDARY; SQUAMOUS CELL CARCINOMA; TRANSGENIC MOUSE; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ADENOCARCINOMA; ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELLS, CULTURED; COLLAGEN; ENZYME INDUCTION; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MALE; MICE, 129 STRAIN; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; PROCOLLAGEN-LYSINE, 2-OXOGLUTARATE 5-DIOXYGENASE; PROMOTER REGIONS, GENETIC; STAT3 TRANSCRIPTION FACTOR; TUMOR MICROENVIRONMENT; UP-REGULATION;

EID: 84924045521     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI74725     Document Type: Article

References (68)

1. Kolacna L, et al. Biochemical and biophysical aspects of collagen nanostructure in the extracellular matrix. Physiol Res. 2007;56(suppl 1):S51-S60.
2. Jodele S, Blavier L, Yoon JM, DeClerck YA. Modifying the soil to affect the seed: r ole of stromal-derived matrix metalloproteinases in cancer progression. Cancer Metastasis Rev. 2006;25(1):35-43.
3. Butcher DT, Alliston T, Weaver VM. A tense situation: forcing tumour progression. Nat Rev Cancer. 2009;9(2):108-122.
4. Yamauchi M, Sricholpech M. Lysine post-translational modifications of collagen. Essays Biochem. 2012;52:113-133.
5. Barker HE, Cox TR, Erler JT. The rationale for targeting the LOX family in cancer. Nat Rev Cancer. 2012;12(8):540-552.
6. Mercer DK, Nicol PF, Kimbembe C, Robins SP. Identifica tion, expression, and tissue distribution of the three rat lysyl hydroxylase isoforms. Biochem Biophys Res Commun. 2003;307(4):803-809.
7. Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M. Lysyl hydroxylase-2b directs collagen cross-linking pathways in MC3T3-E1 cells. J Bone Miner Res. 2004;19(8):1349-1355.
8. Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M. Overexpression of lysyl hydroxylase-2b leads to defective collagen fibrillogenesis and matrix mineralization. J Bone Miner Res. 2005;20(1):81-87.
9. Takalu oma K, Lantto J, Myllyharju J. Lysyl hydroxylase 2 is a specific telopeptide hydroxylase, while all three isoenzymes hydroxylate collagenous sequences. Matrix Biol. 2007;26(5):396-403.
10. Uzawa K, et al. Differential expression of human lysyl hydroxylase genes, lysine hydroxylation, and cross-linking of type I collagen during osteoblastic differentiation in vitro. J Bone Miner Res. 1999;14(8): 1272-1280.
11. van der Slot AJ, et al. Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J Biol Chem. 2003;278(42):40967-40972.
12. Eyre DR,Paz MA,Gallop PM Cross-linking in collagen and elastin Annu Rev Biochem. 1984 53, 717-748.
13. Byers PH, Pyott SM. Recessively inherited forms of osteogenesis imperfecta. Annu Rev Genet. 2012;46:475-497.
14. Seth P, Yeowell HN. Fox-2 protein regulates the alternative splicing of scleroderma-Associated lysyl hydroxylase 2 messenger RNA. Arthritis Rheum. 2010;62(4):1167-1175.
15. Johnson L, et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature. 2001;410(6832):1111-1116.
16. Martin-Caba llero J, Flores JM, Garcia-Palencia P, Serrano M. Tumor susceptibility of p21(Waf1/Cip1)-deficient mice. Cancer Res. 2001;61(16):6234-6238.
17. Yamasaki M, et al. P21 regulates TGF-beta1-induced pulmonary responses via a TNF-?-signaling pathway. Am J Respir Cell Mol Biol. 2008;38(3):346-353.
18. Abbas T, Dutta A. p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer. 2009;9(6):400-414.
19. Warfel NA, El-Deiry WS. p21WAF1 and tumourigenesis: 20 years after. Curr Opin Oncol. 2013;25(1):52-58.
20. Zhu WG, et al. Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21(Cip1) promoter. Mol Cell Biol. 2003;23(12):4056-4065.
21. Adnane J, Jackson RJ, Nicosia SV, Cantor AB, Pl edger WJ, Sebti SM. Loss of p21WAF1/CIP1 accelerates Ras oncogenesis in a transgenic/knockout mammary cancer model. Oncogene. 2000;19(47):5338-5347.
22. Jackson RJ, Engelman RW, Coppola D, Cantor AB, Wharton W, Pledger WJ. p21Cip1 nullizygosity increases tumor metastasis in irradiated mice. Cancer Res. 2003;63(12):3021-3025.
23. Komiya T, et al. p21 expression as a predictor for favorable prognosis in squamous cell carcinoma of the lung. Clin Cancer Res. 1997;3(10):1831-1835.
24. Yeowell HN, Walker LC. Tissue specificity of a new splice form of the human lysyl hydroxylase 2 gene. Matrix Biol. 1999;18(2):179-187.
25. Beer DG, et al. Gene-expression profiles predict survival of patients with lung adenocarcinoma. Nat Med. 2002;8(8):816-824.
26. Bhattacharjee A, et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci U S A. 2001;98(24):13790-13795.
27. Bild AH, et al. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature. 2006;439(7074):353-357.
28. Botling J, et al. Biomarker discovery in non-small cell lung cancer: integrating gene expression profiling, meta-Analysis, and tissue microarray validation. Clin Cancer Res. 2013;19(1):194-204.
29. Chitale D, et al. An integrated genomic analysis of lung cancer reveals loss of DUSP4 in EGFR-mutant tumors. Oncogene. 2009;28(31):2773-2783.
30. Hou J, et al. Gene expre ssion-based classification of non-small cell lung carcinomas and survival prediction. PLoS One. 2010;5(4):e10312.
31. Okayama H, et al. Identification of genes upregulated in ALK-positive and EGFR/KRAS/ALK-negative lung adenocarcinomas. Cancer Res. 2012;72(1):100-111.
32. Director's Challenge Consortium for the Molecular Classification of Lung A, et al. Gene expression-based survival prediction in lung adeno carcinoma: a multi-site, blinded validation study. Nat Med. 2008;14(8):822-827.
33. Tang H, et al. A 12-gene set predicts survival benefits from adjuvant chemotherapy in non-small cell lung cancer patients. Clin Cancer Res. 2013;19(6):1577-1586.
34. Tomida S, et al. Relapse-related molecular signature in lung adenocarcinomas identifies patients with dismal prognosis. J Clin Oncol. 2009;27(17):2793-2799.
35. Zhu CQ, et al. Prognostic and predictive gene signature for adjuvant chemotherapy in resected non-small-cell lung cancer. J Clin Oncol. 2010;28(29):4417-4424.
36. Kessler JD, et al. A SUMOylation-dependent transcriptional subprogram is required for Myc-driven tumorigenesis. Science. 2012;335(6066):348-353.
37. Cancer Genome Atlas Research Net work. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature. 2013;499(7456):43-49.
38. Gilkes DM, et al. Procollagen lysyl hydroxylase 2 is essential for hypoxia-induced breast cancer metastasis. Mol Cancer Res. 2013;11(5):456-466.
39. Roybal JD, et al. miR-200 Inhibits lung adenocarcinoma cell invasion and metastasis by targeting Flt1/VEGFR1. Mol Cancer Res. 2011;9(1):25-35.
40. Pawlus MR, Wang L, Hu CJ. STAT3 and HIF1? cooperatively activate HIF1 target genes in MDA-MB-231 and RCC4 cells. Oncogene. 2014;33(13):1670-1679.
41. Lev ental KR, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 2009;139(5):891-906.
42. Vassallo R. Diffuse lung diseases in cigarette smokers. Semin Respir Crit Care Med. 2012;33(5):533-542.
43. Szauter KM, Cao T, Boyd CD, Csiszar K. Lysyl oxidase in development, aging and pathologies of the skin. Pathol Biol (Paris). 2005;53(7):448-456.
44. Mogi A, Kuwano H. TP53 mutations in nonsmall cell lung cancer. J Biomed Biotechnol. 2011;2011:583929.
45. Jackson JG, Lozano G. The mutant p53 mouse as a pre-clinical model. Oncogene. 2013;32(37):4325-4330.
46. Westcott PM, et al. The mutational landscapes of genetic and chemical models of Kras-driven lung cancer [published online ahead of print No vember 2, 2014]. Nature. doi:10.1038/nature13898.
47. Ling E, Robinson DS. Transforming growth factor-beta1: its anti-inflammatory and pro-fibrotic effects. Clin Exp Allergy. 2002;32(2):175-178.
48. Eisinger-Mathason TS, et al. Hypoxia-dependent modification of collagen networks promotes sarcoma metastasis. Cancer Discov. 2013;3(10):1190-1205.
49. Gilkes DM, et al. Collagen prolyl hydroxylases are essential for breast cancer metastasis. Cancer Res. 2013;73(11):3285-3296.
50. Gilkes DM, Bajpai S, Chaturvedi P, Wirtz D, Semenza GL. Hypoxia-inducible factor 1 (HIF-1) promotes extracellular matrix remodeling under hypoxic conditions by inducing P4HA1, P4HA2, and PLOD2 expression in fibrobla sts. J Biol Chem. 2013;288(15):10819-10829.
51. Nicastri A, et al. N-glycoprotein analysis discovers new up-regulated glycoproteins in colorectal cancer tissue. J Proteome Res. 2014;13(11):4932-4941.
52. Risteli M, Niemitalo O, Lankinen H, Juffer AH, Myllyla R. Characterization of collagenous peptides bound to lysyl hydroxylase isoforms. J Biol Chem. 2004;279(36): 37535-37543.
53. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6(5):392-401.
54. Semenza GL. Cancer-stromal cell interactions mediated by hypoxia-inducible factors promote angiogenesis, lymphangiogenesis, and metastasis. Oncogene. 2013;32(35):4057-4063.
55. Atsawasuwan P,et al Lysyl oxidase binds transforming growth factor-beta and regulates its signaling via amine oxidase activity J Biol Chem. 2008 283 49, 34229-34240.
56. Csisz ar K. Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol. 2001;70:1-32.
57. Decitre M, et al. Lysyl oxidase-like protein localizes to sites of de novo fibri nogenesis in fibrosis and in the early stromal reaction of ductal breast carcinomas. Lab Invest. 1998;78(2):143-151.
58. Tschumperlin DJ, et al. Mechanotransduction through growth-factor shedding into the extracellular space. Nature. 2004;429(6987):83-86.
59. Wipff PJ, Rifkin DB, Meister JJ, Hinz B. Myofibroblast contraction activates latent TGF-?1 from the extracellular matrix. J Cell Biol. 2007;179(6):1311-1323.
60. Wang L, et al. A small molecule modulates Jumonji histone demethylase activity and selectively inhibits cancer growth. Nat Commun. 2013;4:2035.
61. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science. 2005;307(5712):1098-1101.
62. Moff at J, et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral highcontent screen. Cell. 2006;124(6):1283-1298.
63. Creighton CJ, et al. Insulin-like growth fa ctor-I activates gene transcription programs strongly associated with poor breast cancer prognosis. J Clin Oncol. 2008;26(25):4078-4085.
64. Walker LC, Overstreet MA, Yeowell HN. Tissue-specific expression and regulation of the alternatively-spliced forms of lysyl hydroxylase 2 (LH2) in human kidney cells and skin fibroblasts. Matrix Biol. 2005;23(8):515-523.
65. Tang X, et al. Abnormalities of the TITF-1 lineage-specific oncogene in NSCLC: implications in lung cancer pathogenesis and prognosis. Clin Cancer Res. 2011;17(8):2434-2443.
66. Yamauchi M, Shiiba M. Lysine hydroxylation and cross-linking of collagen. Methods Mol Biol. 2008;446:95-108.
67. Zhang N, et al. Overexpression of Separase induces aneuploidy and mammary tumorigenesis. Proc Natl Acad Sci U S A. 2008;105(35):13033-13038.
68. Foty R. A simple hanging drop cell culture protocol for generation of 3D spheroids. J Vis Exp. 2011;(51):2720.