The emerging role of qsox1 in cancer

Antioxidants and Redox Signaling

Volumn 21, Issue 3, 2014, Pages 485-496

  Lake, Douglas F ^a   Faigel, Douglas O ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CETUXIMAB; EVEROLIMUS; PANITUMUMAB; QUIESCIN SULFHYDRYL OXIDASE 1; REGORAFENIB; TEMSIROLIMUS; THIOL OXIDASE; TRASTUZUMAB; UNCLASSIFIED DRUG; OXIDOREDUCTASE; QSOX1 PROTEIN, HUMAN;

BREAST CANCER; CANCER PROGNOSIS; CARCINOGENESIS; CELL MIGRATION; COLORECTAL CANCER; CRYSTAL STRUCTURE; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FIBROBLAST; METASTASIS POTENTIAL; NEOPLASM; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; REVIEW; STROMA CELL; TUMOR CELL; BIOSYNTHESIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY;

CARCINOGENESIS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASMS; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS;

EID: 84900513040     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5572     Document Type: Review

References (86)

1. American Cancer Society American Cancer Society. 2013. www.cancer.org/research/cancerfactsstatistics/cancerfactsfigures2013/ index. Accessed July 10 2013.
2. Agarwala SS and Case S. Everolimus (RAD001) in the treatment of advanced renal cell carcinoma: a review. Oncologist 15: 236-245, 2010.
3. Ahmad SS, Duke S, Jena R, Williams MV, and Burnet NG. Advances in radiotherapy. BMJ 345: e7765, 2012.
4. Al-Sohaily S, Biankin A, Leong R, Kohonen-Corish M, and Warusavitarne J. Molecular pathways in colorectal cancer. J Gastroenterol Hepatol 27: 1423-1431, 2012.
5. Alon A, Grossman I, Gat Y, Kodali VK, DiMaio F, Mehlman T, Haran G, Baker D, Thorpe C, and Fass D. The dynamic disulphide relay of quiescin sulphydryl oxidase. Nature 488: 414-418, 2012.
6. Alon A, Heckler EJ, Thorpe C, and Fass D. QSOX contains a pseudo-dimer of functional and degenerate sulfhydryl oxidase domains. FEBS Lett 584: 1521-1525, 2010.
7. Antwi K, Hostetter G, Demeure M, Decker G, Ruiz Y, Sielaff T, Koep L, and Lake D. Analysis of human plasma peptidome reveals potential biomarker for pancreatic cancer. J Proteome Res 8: 4722-4731, 2009.
8. Aokage K, Ishii G, Ohtaki Y, Yamaguchi Y, Hishida T, Yoshida J, Nishimura M, Nagai K, and Ochiai A. Dynamic molecular changes associated with epithelial-mesenchymal transition and subsequent mesenchymal-epithelial transition in the early phase of metastatic tumor formation. Int J Cancer 128: 1585-1595, 2010.
9. Arbiser JL, Petros J, Klafter R, Govindajaran B, McLaughlin ER, Brown LF, Cohen C, Moses M, Kilroy S, Arnold RS, and Lambeth JD. Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc Natl Acad Sci U S A 99: 715-720, 2002.
10. Asatiani E, Huang WX, Wang A, Rodriguez Ortner E, Cavalli LR, Haddad BR, and Gelmann EP. Deletion, methylation, and expression of the NKX3.1 suppressor gene in primary human prostate cancer. Cancer Res 65: 1164-1173, 2005.
11. Ashman LK and Griffith R. Therapeutic targeting of c-KIT in cancer. Expert Opin Investig Drugs 22: 103-115, 2013.
12. Berquist BR and Wilson DM, 3rd. Pathways for repairing and tolerating the spectrum of oxidative DNA lesions. Cancer Lett 327: 61-72, 2012.
13. Blick T, Widodo E, Hugo H, Waltham M, Lenburg ME, Neve RM, and Thompson EW. Epithelial mesenchymal transition traits in human breast cancer cell lines. Clin Exp Metastasis 25: 629-642, 2008.
14. Box C, Rogers SJ, Mendiola M, and Eccles SA. Tumourmicroenvironmental interactions: paths to progression and targets for treatment. Semin Cancer Biol 20: 128-138, 2010.
15. Cannito S, Novo E, Compagnone A, Valfre di Bonzo L, Busletta C, Zamara E, Paternostro C, Povero D, Bandino A, Bozzo F, Cravanzola C, Bravoco V, Colombatto S, and Parola M. Redox mechanisms switch on hypoxia-dependent epithelial-mesenchymal transition in cancer cells. Carcinogenesis 29: 2267-2278, 2008.
16. Cannito S, Novo E, di Bonzo LV, Busletta C, Colombatto S, and Parola M. Epithelial-mesenchymal transition: from molecular mechanisms, redox regulation to implications in human health and disease. Antioxid Redox Signal 12: 1383-1430, 2010.
17. Cano CE, Gommeaux J, Pietri S, Culcasi M, Garcia S, Seux M, Barelier S, Vasseur S, Spoto RP, Pebusque MJ, Dusetti NJ, Iovanna JL, and Carrier A. Tumor protein 53-induced nuclear protein 1 is a major mediator of p53 antioxidant function. Cancer Res 69: 219-226, 2009.
18. Chiarugi P and Buricchi F. Protein tyrosine phosphorylation and reversible oxidation: two cross-talking posttranslation modifications. Antioxid Redox Signal 9: 1-24, 2007.
19. Chiu J and Dawes IW. Redox control of cell proliferation. Trends Cell Biol 22: 592-601, 2012.
20. Coppock DL, Cina-Poppe D, and Gilleran S. The quiescin Q6 gene (QSCN6) is a fusion of two ancient gene families: thioredoxin and ERV1. Genomics 54: 460-468, 1998.
21. Coppock DL, Kopman C, Scandalis S, and Gilleran S. Preferential gene expression in quiescent human lung fibroblasts. Cell Growth Differ 4: 483-493, 1993.
22. Coppock DL and Thorpe C. Multidomain flavin-dependent sulfhydryl oxidases. Antioxid Redox Signal 8: 300-311, 2006.
23. Das P, Siegers GM, and Postovit LM. Illuminating luminal B: QSOX1 as a subtype-specific biomarker. Breast Cancer Res 15: 104, 2013.
24. DeGrado TR, Turkington TG, Williams JJ, Stearns CW, Hoffman JM, and Coleman RE. Performance characteristics of a whole-body PET scanner. J Nucl Med 35: 1398-1406, 1994.
25. Deininger MW and Druker BJ. Specific targeted therapy of chronic myelogenous leukemia with imatinib. Pharmacol Rev 55: 401-423, 2003.
26. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, Paz B, Shen J, Lau SK, Quake SR, Brown JM, Weissman IL, and Clarke MF. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458: 780-783, 2009.
27. Esposito F, Ammendola R, Faraonio R, Russo T, and Cimino F. Redox control of signal transduction, gene expression and cellular senescence. Neurochem Res 29: 617-628, 2004.
28. Foulkes WD. Inherited susceptibility to common cancers. N Engl J Med 359: 2143-2153, 2008.
29. Freed-Pastor WA and Prives C. Mutant p53: one name, many proteins. Genes Dev 26: 1268-1286, 2012.
30. Gilbert HF. Protein disulfide isomerase and assisted protein folding. J Biol Chem 272: 29399-29402, 1997.
31. Go YM and Jones DP. Redox control systems in the nucleus: mechanisms and functions. Antioxid Redox Signal 13: 489-509, 2010.
32. Goldman L and Schafer AI (Eds). Goldmans's Cecil Medicine. Philadelphia: Saunders, 2012
33. Grothey A, Van Cutsem E, Sobrero A, Siena S, Falcone A, Ychou M, Humblet Y, Bouche O, Mineur L, Barone C, Adenis A, Tabernero J, Yoshino T, Lenz HJ, Goldberg RM, Sargent DJ, Cihon F, Cupit L, Wagner A, and Laurent D. Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet 381: 303-312, 2013.
34. He WW, Sciavolino PJ, Wing J, Augustus M, Hudson P, Meissner PS, Curtis RT, Shell BK, Bostwick DG, Tindall DJ, Gelmann EP, Abate-Shen C, and Carter KC. A novel human prostate-specific, androgen-regulated homeobox gene (NKX3.1) that maps to 8p21, a region frequently deleted in prostate cancer. Genomics 43: 69-77, 1997.
35. Heckler EJ, Alon A, Fass D, and Thorpe C. Human quiescin-sulfhydryl oxidase, QSOX1: probing internal redox steps by mutagenesis. Biochemistry 47: 4955-4963, 2008.
36. Hellebrekers DM, Melotte V, Viré E, Langenkamp E, Molema G, Fuks F, Herman JG, Van Criekinge W, Griffioen AW, and van Engeland M. Identification of epigenetically silenced genes in tumor endothelial cells. Cancer Res 67: 4138-4148, 2007.
37. Hernandez-Aya LF and Gonzalez-Angulo AM. Adjuvant systemic therapies in breast cancer. Surg Clin North Am 93: 473-491, 2013.
38. Hoober KL, Glynn NM, Burnside J, Coppock DL, and Thorpe C. Homology between egg white sulfhydryl oxidase and quiescin Q6 defines a new class of flavin-linked sulfhydryl oxidases. J Biol Chem 274: 31759-31762, 1999.
39. Hoober KL, Joneja B, White HB, 3rd, and Thorpe C. A sulfhydryl oxidase from chicken egg white. J Biol Chem 271: 30510-30516, 1996.
40. Hoober KL, Sheasley SL, Gilbert HF, and Thorpe C. Sulfhydryl oxidase from egg white. A facile catalyst for disulfide bond formation in proteins and peptides. J Biol Chem 274: 22147-22150, 1999.
41. Hoober KL and Thorpe C. Egg white sulfhydryl oxidase: kinetic mechanism of the catalysis of disulfide bond formation. Biochemistry 38: 3211-3217, 1999.
42. Hoober KL and Thorpe C. Flavin-dependent sulfhydryl oxidases in protein disulfide bond formation. Methods Enzymol 348: 30-34, 2002.
43. Huang L, Lou CH, Chan W, Shum EY, Shao A, Stone E, Karam R, Song HW, and Wilkinson MF. RNA homeostasis governed by cell type-specific and branched feedback loops acting on NMD. Mol Cell 43: 950-961, 2011.
44. Ilani T, Alon A, Grossman I, Horowitz B, Kartvelishvily E, Cohen SR, and Fass D. A Secreted disulfide catalyst controls extracellular matrix composition and function. Science 341: 74-76, 2013.
45. Iwao-Koizumi K, Matoba R, Ueno N, Kim SJ, Ando A, Miyoshi Y, Maeda E, Noguchi S, and Kato K. Prediction of docetaxel response in human breast cancer by gene expression profiling. J Clin Oncol 23: 422-431, 2005.
46. Katchman BA, Antwi K, Hostetter G, Demeure MJ, Watanabe A, Decker GA, Miller LJ, Von Hoff DD, and Lake DF. Quiescin sulfhydryl oxidase 1 promotes invasion of pancreatic tumor cells mediated by matrix metalloproteinases. Mol Cancer Res MCR 9: 1621-1631, 2011.
47. Katchman BA, Ocal IT, Cunliffe HE, Chang YH, Hostetter G, Watanabe A, Lobello J, and Lake DF. Expression of quiescin sulfhydryl oxidase 1 is associated with a highly invasive phenotype and correlates with a poor prognosis in Luminal B breast cancer. Breast Cancer Res 15: R28, 2013.
48. Kim SH, Turnbull J, and Guimond S. Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J Endocrinol 209: 139-151, 2011.
49. Kodali VK and Thorpe C. Quiescin sulfhydryl oxidase from Trypanosoma brucei: catalytic activity and mechanism of a QSOX family member with a single thioredoxin domain. Biochemistry 49: 2075-2085, 2010.
50. Lambrechts D, Lenz HJ, de Haas S, Carmeliet P, and Scherer SJ. Markers of response for the antiangiogenic agent bevacizumab. J Clin Oncol 31: 1219-1230, 2013.
51. Landriscina M, Maddalena F, Laudiero G, and Esposito F. Adaptation to oxidative stress, chemoresistance, and cell survival. Antioxid Redox Signal 11: 2701-2716, 2009.
52. Lee J, Hofhaus G, and Lisowsky T. Erv1p from Saccharomyces cerevisiae is a FAD-linked sulfhydryl oxidase. FEBS Lett 477: 62-66, 2000.
53. Macoska JA, Trybus TM, Benson PD, Sakr WA, Grignon DJ, Wojno KD, Pietruk T, and Powell IJ. Evidence for three tumor suppressor gene loci on chromosome 8p in human prostate cancer. Cancer Res 55: 5390-5395, 1995.
54. Michl P and Gress TM. Current concepts and novel targets in advanced pancreatic cancer. Gut 62: 317-326, 2013.
55. Mohamed A, Krajewski K, Cakar B, and Ma CX. Targeted therapy for breast cancer. Am J Pathol 183: 1096-1112, 2013.
56. Morel C, Adami P, Musard JF, Duval D, Radom J, and Jouvenot M. Involvement of sulfhydryl oxidase QSOX1 in the protection of cells against oxidative stress-induced apoptosis. Exp Cell Res 313: 3971-3982, 2007.
57. Murphy ME. The HSP70 family and cancer. Carcinogenesis 34: 1181-1188, 2013.
58. Nambiar M and Raghavan SC. How does DNA break during chromosomal translocations. Nucl Acids Res 39: 5813-5825, 2011.
59. Oliveira-Marques V, Marinho HS, Cyrne L, and Antunes F. Role of hydrogen peroxide in NF-kappaB activation: from inducer to modulator. Antioxid Redox Signal 11: 2223-2243, 2009.
60. Padgett RA. New connections between splicing and human disease. Trends Genet: TIG 28: 147-154, 2012.
61. Palmieri C, Patten DK, Januszewski A, Zucchini G, and Howell SJ. Breast cancer: current and future endocrine therapies. Mol Cell Endocrinol 382: 695-723, 2013.
62. Pani G, Galeotti T, and Chiarugi P. Metastasis: cancer cell's escape from oxidative stress. Cancer Metastasis Rev 29: 351-378, 2010.
63. Pani G, Giannoni E, Galeotti T, and Chiarugi P. Redoxbased escape mechanism from death: the cancer lesson. Antioxid Redox Signal 11: 2791-2806, 2009.
64. Papavasiliou P, Chun YS, and Hoffman JP. How to define and manage borderline resectable pancreatic cancer. Surg Clin North Am 93: 663-674, 2013.
65. Patel SG and Ahnen DJ. Familial colon cancer syndromes: an update of a rapidly evolving field. Curr Gastroenterol Rep 14: 428-438, 2012.
66. Pelicano H, Carney D, and Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist Updat 7: 97-110, 2004.
67. Pernodet N, Hermetet F, Adami P, Vejux A, Descotes F, Borg C, Adams M, Pallandre JR, Viennet G, Esnard F, Jouvenot M, and Despouy G. High expression of QSOX1 reduces tumorogenesis, and is associated with a better outcome for breast cancer patients. Breast Cancer Res 14: R136, 2012.
68. Portes KF, Ikegami CM, Getz J, Martins AP, de Noronha L, Zischler LF, Klassen G, Camargo AA, Zanata SM, Bevilacqua E, and Nakao LS. Tissue distribution of quiescin Q6/sulfhydryl oxidase (QSOX) in developing mouse. J Mol Histol 39: 217-225, 2008.
69. Radisky ES and Radisky DC. Matrix metalloproteinaseinduced epithelial-mesenchymal transition in breast cancer. J mammary Gland Biol Neoplasia 15: 201-212, 2010.
70. Raje S, Glynn NM, and Thorpe C. A continuous fluorescence assay for sulfhydryl oxidase. Anal Biochem 307: 266-272, 2002.
71. Rancy PC and Thorpe C. Oxidative protein folding in vitro: a study of the cooperation between quiescin-sulfhydryl oxidase and protein disulfide isomerase. Biochemistry 47: 12047-12056, 2008.
72. Reinhold WC, Sunshine M, Liu H, Varma S, Kohn KW, Morris J, Doroshow J, and Pommier Y. CellMiner: a webbased suite of genomic and pharmacologic tools to explore transcript and drug patterns in the NCI-60 cell line set. Cancer Res 72: 3499-3511, 2012.
73. Riemer J, Bulleid N, and Herrmann JM. Disulfide formation in the ER and mitochondria: two solutions to a common process. Science 324: 1284-1287, 2009.
74. Rudolf J, Pringle MA, and Bulleid NJ. Proteolytic processing of QSOX1A ensures efficient secretion of a potent disulfide catalyst. Biochem J 454: 181-190, 2013.
75. Sanchez-Munoz A, Perez-Ruiz E, Jimenez B, Ribelles N, Marquez A, Garcia-Rios I, and Alba Conejo E. Targeted therapy of metastatic breast cancer. Clin Transl Oncol 11: 643-650, 2009.
76. Sekhar KR, Rachakonda G, and Freeman ML. Cysteinebased regulation of the CUL3 adaptor protein Keap1. Toxicol Appl Pharmacol 244: 21-26, 2010.
77. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, and McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235: 177-182, 1987.
78. Soloviev M, Esteves MP, Amiri F, Crompton MR, and Rider CC. Elevated transcription of the gene QSOX1 encoding quiescin Q6 sulfhydryl oxidase 1 in breast cancer. PloS One 8: e57327, 2013.
79. Song H, Zhang B, Watson MA, Humphrey PA, Lim H, and Milbrandt J. Loss of Nkx3.1 leads to the activation of discrete downstream target genes during prostate tumorigenesis. Oncogene 28: 3307-3319, 2009.
80. Sounni NE and Noel A. Targeting the tumor microenvironment for cancer therapy. Clin Chem 59: 85-93, 2013.
81. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, and Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270: 296-299, 1995.
82. Thorpe C, Hoober KL, Raje S, Glynn NM, Burnside J, Turi GK, and Coppock DL. Sulfhydryl oxidases: emerging catalysts of protein disulfide bond formation in eukaryotes. Arch Biochem Biophys 405: 1-12, 2002.
83. Tol J and Punt CJ. Monoclonal antibodies in the treatment of metastatic colorectal cancer: a review. Clin Ther 32: 437-453, 2010.
84. Truong TH and Carroll KS. Redox regulation of epidermal growth factor receptor signaling through cysteine oxidation. Biochemistry 51: 9954-9965, 2012.
85. Tury A, Mairet-Coello G, Poncet F, Jacquemard C, Risold PY, Fellmann D, and Griffond B. QSOX sulfhydryl oxidase in rat adenohypophysis: localization and regulation by estrogens. J Endocrinol 183: 353-363, 2004.
86. Wong GS and Rustgi AK. Matricellular proteins: priming the tumour microenvironment for cancer development and metastasis. Br J Cancer 108: 755-761, 2013.