Benzene metabolite hydroquinone up-regulates chondromodulin-I and inhibits tube formation in human bone marrow endothelial cells

Molecular Pharmacology

Volumn 76, Issue 3, 2009, Pages 579-587

  Zhou, Hongfei ^a   Kepa, Jadwiga K ^a   Siegel, David ^a   Miura, Shigenori ^b   Hiraki, Yuji ^b   Ross, David ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BENZENE DERIVATIVE; CHONDROMODULIN 1; CYTOKINE; HYDROQUINONE; MESSENGER RNA; RECOMBINANT PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (QUINONE); SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; BONE MARROW CELL; BONE MARROW TOXICITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION;

BENZENE; BONE MARROW CELLS; CELL LINE; COLLAGEN; DRUG COMBINATIONS; ENDOTHELIAL CELLS; HUMANS; HYDROQUINONES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LAMININ; MEMBRANE PROTEINS; NAD(P)H DEHYDROGENASE (QUINONE); PROTEOGLYCANS; RNA, MESSENGER; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 69549083468     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.109.057323     Document Type: Article

References (40)

1. Aoyama T, Okamoto T, Nagayama S, Nishijo K, Ishibe T, Yasura K, Nakayama T, Nakamura T, and Toguchida J (2004) Methylation in the core-promoter region of the chondromodulin-I gene determines the cell-specific expression by regulating the binding of transcriptional activator Sp3. J Biol Chem 279:28789-28797. (Pubitemid 38900164)
2. Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, Jin DK, Dias S, Zhang F, Hartman TE, et al. (2004) Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med 10:64-71. (Pubitemid 38524700)
3. Azizan A, Holaday N, and Neame PJ (2001) Post-translational processing of bovine chondromodulin-I. J Biol Chem 276:23632-23638.
4. Bauer AK, Faiola B, Abernethy DJ, Marchan R, Pluta LJ, Wong VA, Roberts K, Jaiswal AK, Gonzalez FJ, Butterworth BE, et al. (2003) Genetic susceptibility to benzene-induced toxicity: role of NADPH:quinone oxidoreductase-1. Cancer Res 63:929-935. (Pubitemid 36278421)
5. Bironaite D, Siegel D, Moran JL, Weksler BB, and Ross D (2004) Stimulation of endothelial IL-8 (eIL-8) production and apoptosis by phenolic metabolites of benzene in HL-60 cells and human bone marrow endothelial cells. Chem Biol Interact 149:177-188. (Pubitemid 39061046)
6. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S, Cavallo D, Byun HM, Jiang J, Marinelli B, Pesatori AC, et al. (2007) Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res 67:876-880. (Pubitemid 46270740)
7. Caplan AI and Dennis JE (2006) Mesenchymal stem cells as trophic mediators. J Cell Biochem 98:1076-1084. (Pubitemid 44128350)
8. Davis GE, Koh W, and Stratman AN (2007) Mechanisms controlling human endothelial lumen formation and tube assembly in three-dimensional extracellular matrices. Birth Defects Res C Embryo Today 81:270-285.
9. Dexter TM, Allen TD, and Lajtha LG (1977) Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol 91:335-344. (Pubitemid 8112206)
10. Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, and Keiliss-Borok IV (1974) Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17:331-340.
11. Hiraki Y, Mitsui K, Endo N, Takahashi K, Hayami T, Inoue H, Shukunami C, Tokunaga K, Kono T, Yamada M, et al. (1999) Molecular cloning of human chondromodulin-I, a cartilage-derived growth modulating factor, and its expression in Chinese hamster ovary cells. Eur J Biochem 260:869-878. (Pubitemid 29148655)
12. Hiraki Y and Shukunami C (2000) Chondromodulin-I as a novel cartilage-specific growth-modulating factor. Pediatr Nephrol 14:602-605. (Pubitemid 30394436)
13. Hiraki Y and Shukunami C (2005) Angiogenesis inhibitors localized in hypovascular mesenchymal tissues: chondromodulin-I and tenomodulin. Connect Tissue Res 46:3-11. (Pubitemid 40823576)
14. Hiraki Y, Tanaka H, Inoue H, Kondo J, Kamizono A, and Suzuki F (1991) Molecular cloning of a new class of cartilage-specific matrix, chondromodulin-I, which stimulates growth of cultured chondrocytes. Biochem Biophys Res Commun 175:971-977.
15. Kopp HG, Avecilla ST, Hooper AT, and Rafii S (2005) The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda) 20:349-356.
16. Lan Q, Zhang L, Li G, Vermeulen R, Weinberg RS, Dosemeci M, Rappaport SM, Shen M, Alter BP, Wu Y, et al. (2004) Hematotoxicity in workers exposed to low levels of benzene. Science 306:1774-1776. (Pubitemid 39601394)
17. Li Z and Li L (2006) Understanding hematopoietic stem-cell microenvironments. Trends Biochem Sci 31:589-595.
18. Lowry OH, Rosebrough NJ, Farr AL, and Randall RJ (1951) Protein measurement with Folin phenol reagent. J Biol Chem 193:265-267.
19. Matsumura T, Wolff K, and Petzelbauer P (1997) Endothelial cell tube formation depends on cadherin 5 and CD31 interactions with filamentous actin. J Immunol 158:3408-3416. (Pubitemid 127484061)
20. Moran JL, Siegel D, and Ross D (1999) A potential mechanism underlying the increased susceptibility of individuals with a polymorphism in NAD(P)H:quinone oxidoreductase 1 (NQO1) to benzene toxicity. Proc Natl Acad Sci U S A 96:8150-8155. (Pubitemid 29328423)
21. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63.
22. Oshima Y, Sato K, Tashiro F, Miyazaki J, Nishida K, Hiraki Y, Tano Y, and Shukunami C (2004) Anti-angiogenic action of the C-terminal domain of tenomodulin that shares homology with chondromodulin-I. J Cell Sci 117:2731-2744. (Pubitemid 38997256)
23. Rickert DE, Baker TS, Bus JS, Barrow CS, and Irons RD (1979) Benzene disposition in the rat after exposure by inhalation. Toxicol Appl Pharmacol 49:417-423.
24. Ross D (1996) Metabolic basis of benzene toxicity. Eur J Haematol Suppl 60:111-118.
25. Ross D (1997) Quinone reductases, in Comprehensive Toxicology, Volume 3: Biotransformation (Guengerich FP ed) pp 179-198, Pergamon, New York.
26. Ross D (2000) The role of metabolism and specific metabolites in benzene-induced toxicity: evidence and issues. J Toxicol Environ Health A 61:357-372.
27. Ross D (2005) Functions and distribution of NQO1 in human bone marrow: potential clues to benzene toxicity. Chem Biol Interact 153-154:137-146.
28. Ross D, Traver RD, Siegel D, Kuehl BL, Misra V, and Rauth AM (1996) A polymorphism in NAD(P)H:quinone oxidoreductase (NQO1): relationship of a homozygous mutation at position 609 of the NQO1 cDNA to NQO1 activity. Br J Cancer 74:995-996. (Pubitemid 26319344)
29. Rothman N, Smith MT, Hayes RB, Traver RD, Hoener B, Campleman S, Li GL, Dosemeci M, Linet M, Zhang L, et al. (1997) Benzene poisoning, a risk factor for hematological malignancy, is associated with the NQO1 609C→T mutation and rapid fractional excretion of chlorzoxazone. Cancer Res 57:2839-2842. (Pubitemid 27315023)
30. Schweitzer KM, Vicart P, Delouis C, Paulin D, Dräger AM, Langenhuijsen MM, and Weksler BB (1997) Characterization of a newly established human bone marrow endothelial cell line: distinct adhesive properties for hematopoietic progenitors compared with human umbilical vein endothelial cells. Lab Invest 76:25-36. (Pubitemid 27058195)
31. Setoguchi K, Misaki Y, Kawahata K, Shimada K, Juji T, Tanaka S, Oda H, Shukunami C, Nishizaki Y, Hiraki Y, et al. (2004) Suppression of T cell responses by chondromodulin I, a cartilage-derived angiogenesis inhibitory factor: therapeutic potential in rheumatoid arthritis. Arthritis Rheum 50:828-839. (Pubitemid 38326183)
32. Shukunami C and Hiraki Y (2007) Chondromodulin-I and tenomodulin: the negative control of angiogenesis in connective tissue. Curr Pharm Des 13:2101-2112. (Pubitemid 47040491)
33. Stillman WS, Varella-Garcia M, Gruntmeir JJ, and Irons RD (1997) The benzene metabolite, hydroquinone, induces dose-dependent hypoploidy in a human cell line. Leukemia 11:1540-1545. (Pubitemid 27404397)
34. Travis LB, Li CY, Zhang ZN, Li DG, Yin SN, Chow WH, Li GL, Dosemeci M, Blot W, and Fraumeni JF Jr. (1994) Hematopoietic malignancies and related disorders among benzene-exposed workers in China. Leuk Lymphoma 14:91-102. (Pubitemid 24197029)
35. Vichai V and Kirtikara K (2006) Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc 1:1112-1116.
36. Winski SL, Hargreaves RH, Butler J, and Ross D (1998) A new screening system for NAD(P)H:quinone oxidoreductase (NQO1)-directed antitumor quinones: identification of a new aziridinylbenzoquinone, RH1, as a NQO1-directed antitumor agent. Clin Cancer Res 4:3083-3088. (Pubitemid 29001485)
37. Yanagihara I, Yamagata M, Sakai N, Shukunami C, Kurahashi H, Yamazaki M, Michigami T, Hiraki Y, and Ozono K (2000) Genomic organization of the human chondromodulin-1 gene containing a promoter region that confers the expression of reporter gene in chondrogenic ATDC5 cells. J Bone Miner Res 15:421-429. (Pubitemid 30134086)
38. Yoshioka M, Yuasa S, Matsumura K, Kimura K, Shiomi T, Kimura N, Shukunami C, Okada Y, Mukai M, Shin H, et al. (2006) Chondromodulin-I maintains cardiac valvular function by preventing angiogenesis. Nat Med 12:1151-1159. (Pubitemid 44527350)
39. Zheng JH, Pyatt DW, Gross SA, Le AT, Kerzic PJ, and Irons RD (2004) Hydroquinone modulates the GM-CSF signaling pathway in TF-1 cells. Leukemia 18:1296-1304.
40. Zhou H, Kepa J, Siegel D, Hiraki Y, and Ross D (2008) Benzene metabolite hydroquinone up-regulates chondromodulin I and inhibits tube formation in human bone marrow endothelial cells (Abstract), in Proceedings of the 99th Annual Meeting of the American Association for Cancer Research; 2008 Apr 12-16; San Diego, CA. p. 608. American Association for Cancer Research, Philadelphia.