Heme oxygenase-1 and its metabolites affect pancreatic tumor growth in vivo

Molecular Cancer

Volumn 8, Issue , 2009, Pages

  Nuhn, Philipp ^a   Künzli, Beat M ^a   Hennig, René ^a   Mitkus, Tomas ^b   Ramanauskas, Tadas ^b   Nobiling, Rainer ^b   Meuer, Stefan C ^b   Friess, Helmut ^a   Berberat, Pascal O ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BILIVERDIN; CARBON MONOXIDE; DEFEROXAMINE; GEMCITABINE; HEME OXYGENASE 1; IRON; PROTOPORPHYRIN COBALT; PROTOPORPHYRIN ZINC; COBALT; SIDEROPHORE; ZINC;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG RESISTANCE; DRUG SENSITIVITY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; IRON DEPLETION; MOUSE; NONHUMAN; PANCREAS CANCER; TUMOR VOLUME; ANALYSIS OF VARIANCE; ANIMAL; CANCER TRANSPLANTATION; DISEASE MODEL; FEMALE; GENETICS; HUMAN; METABOLISM; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; TUMOR CELL LINE;

AGOUTI PACA; MURINAE;

ANALYSIS OF VARIANCE; ANIMALS; BILIVERDINE; CARBON MONOXIDE; CELL LINE, TUMOR; CELL PROLIFERATION; COBALT; DEFEROXAMINE; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; FEMALE; HEME OXYGENASE-1; HUMANS; IRON; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; PANCREATIC NEOPLASMS; SIDEROPHORES; ZINC;

EID: 67650093930     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-8-37     Document Type: Article

References (49)

1. Jemal A Siegel R Ward E Murray T Xu J Thun MJ Cancer statistics, 2007 CA Cancer J Clin 2007, 57:43-66. 10.3322/canjclin.57.1.43 17237035
2. Ghaneh P Slavin J Sutton R Hartley M Neoptolemos JP Adjuvant therapy in pancreatic cancer World J Gastroenterol 2001, 7:482-489. 11819814
3. Otterbein LE Choi AM Heme oxygenase: Colors of defense against cellular stress Am J Physiol Lung Cell Mol Physiol 2000, 279:L1029-1037. 11076792
4. Maines MD The heme oxygenase system: A regulator of second messenger gases Annu Rev Pharmacol Toxicol 1997, 37:517-554. 10.1146/ annurev.pharmtox.37.1.517 9131263
5. Schacter BA Heme catabolism by heme oxygenase: Physiology, regulation, and mechanism of action Semin Hematol 1988, 25:349-369. 3064316
6. Otterbein LE Bach FH Alam J Soares M Tao Lu H Wysk M Davis RJ Flavell RA Choi AM Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway Nat Med 2000, 6:422-428. 10.1038/74680 10742149
7. Berberat PO Katori M Kaczmarek E Anselmo D Lassman C Ke B Shen X Busuttil RW Yamashita K Csizmadia E et al. Heavy chain ferritin acts as an antiapoptotic gene that protects livers from ischemia reperfusion injury Faseb J 2003, 17:1724-1726. 12958189
8. Pae HO Oh GS Choi BM Chae SC Kim YM Chung KR Chung HT Carbon monoxide produced by heme oxygenase-1 suppresses T cell proliferation via inhibition of IL-2 production J Immunol 2004, 172:4744-4751. 15067050
9. Otterbein LE Soares MP Yamashita K Bach FH Heme oxygenase-1: Unleashing the protective properties of heme Trends Immunol 2003, 24:449-455. 10.1016/S1471-4906(03)00181-9 12909459
10. Sunamura M Duda DG Ghattas MH Lozonschi L Motoi F Yamauchi J Matsuno S Shibahara S Abraham NG Heme oxygenase-1 accelerates tumor angiogenesis of human pancreatic cancer Angiogenesis 2003, 6:15-24. 10.1023/ A:1025803600840 14517400
11. Elbirt KK Whitmarsh AJ Davis RJ Bonkovsky HL Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells. Role of mitogen-activated protein kinases J Biol Chem 1998, 273:8922-8931. 10.1074/jbc.273.15.8922 9535875
12. Tanaka S Akaike T Fang J Beppu T Ogawa M Tamura F Miyamoto Y Maeda H Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour Br J Cancer 2003, 88:902-909. 10.1038/ sj.bjc.6600830 12644828
13. Goodman AI Choudhury M da Silva JL Schwartzman ML Abraham NG Overexpression of the heme oxygenase gene in renal cell carcinoma Proc Soc Exp Biol Med 1997, 214:54-61. 9012361
14. Maines MD Abrahamsson PA Expression of heme oxygenase-1 (HSP32) in human prostate: Normal, hyperplastic, and tumor tissue distribution Urology 1996, 47:727-733. 10.1016/S0090-4295(96)00010-6 8650873
15. Schacter BA Kurz P Alterations in microsomal drug metabolism and heme oxygenase activity in isolated hepatic parenchymal and sinusoidal cells in Murphy-Sturm lymphosarcoma-bearing rats Clin Invest Med 1986, 9:150-155. 3093126
16. Berberat PO Dambrauskas Z Gulbinas A Giese T Giese N Kunzli B Autschbach F Meuer S Buchler MW Friess H Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment Clin Cancer Res 2005, 11:3790-3798. 10.1158/1078-0432.CCR-04-2159 15897578
17. Christova TY Gorneva GA Taxirov SI Duridanova DB Setchenska MS Effect of cisplatin and cobalt chloride on antioxidant enzymes in the livers of Lewis lung carcinoma-bearing mice: Protective role of heme oxygenase Toxicol Lett 2003, 138:235-242. 10.1016/S0378-4274(02)00416-2 12565200
18. Doi K Akaike T Fujii S Tanaka S Ikebe N Beppu T Shibahara S Ogawa M Maeda H Induction of haem oxygenase-1 nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth Br J Cancer 1999, 80:1945-1954. 10.1038/sj.bjc.6690624 10471043
19. Fang J Sawa T Akaike T Akuta T Sahoo SK Khaled G Hamada A Maeda H In vivo antitumor activity of pegylated zinc protoporphyrin: Targeted inhibition of heme oxygenase in solid tumor Cancer Res 2003, 63:3567-3574. 12839943
20. Hancock WW Buelow R Sayegh MH Turka LA Antibody-induced transplant arteriosclerosis is prevented by graft expression of anti-oxidant and anti-apoptotic genes Nat Med 1998, 4:1392-1396. 10.1038/3982 9846576
21. Willis D Moore AR Frederick R Willoughby DA Heme oxygenase: A novel target for the modulation of the inflammatory response Nat Med 1996, 2:87-90. 10.1038/nm0196-87 8564848
22. Hennig R Ventura J Segersvard R Ward E Ding XZ Rao SM Jovanovic BD Iwamura T Talamonti MS Bell RH Jr Adrian TE LY293111 improves efficacy of gemcitabine therapy on pancreatic cancer in a fluorescent orthotopic model in athymic mice Neoplasia 2005, 7:417-425. 1501143 15967119 10.1593/neo.04559
23. Durante W Heme oxygenase-1 in growth control and its clinical application to vascular disease J Cell Physiol 2003, 195:373-382. 10.1002/jcp.10274 12704646
24. Katori M Buelow R Ke B Ma J Coito AJ Iyer S Southard D Busuttil RW Kupiec-Weglinski JW Heme oxygenase-1 overexpression protects rat hearts from cold ischemia/reperfusion injury via an antiapoptotic pathway Transplantation 2002, 73:287-292. 10.1097/00007890-200201270-00023 11821745
25. Ryter SW Otterbein LE Carbon monoxide in biology and medicine Bioessays 2004, 26:270-280. 10.1002/bies.20005 14988928
26. Yet SF Tian R Layne MD Wang ZY Maemura K Solovyeva M Ith B Melo LG Zhang L Ingwall JS et al. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice Circ Res 2001, 89:168-173. 10.1161/hh1401.093314 11463724
27. Otterbein LE Kolls JK Mantell LL Cook JL Alam J Choi AM Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury J Clin Invest 1999, 103:1047-1054. 408257 10194478 10.1172/JCI5342
28. Torisu-Itakura H Furue M Kuwano M Ono M Co-expression of thymidine phosphorylase and heme oxygenase-1 in macrophages in human malignant vertical growth melanomas Jpn J Cancer Res 2000, 91:906-910. 11011118
29. Nishie A Ono M Shono T Fukushi J Otsubo M Onoue H Ito Y Inamura T Ikezaki K Fukui M et al. Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas Clin Cancer Res 1999, 5:1107-1113. 10353745
30. Hirai K Sasahira T Ohmori H Fujii K Kuniyasu H Inhibition of heme oxygenase-1 by zinc protoporphyrin IX reduces tumor growth of LL/2 lung cancer in C57BL mice Int J Cancer 2007, 120:500-505. 10.1002/ijc.22287 17066448
31. Nair P Muthukkumar S Sells SF Han SS Sukhatme VP Rangnekar VM Early growth response-1-dependent apoptosis is mediated by p53 J Biol Chem 1997, 272:20131-20138. 10.1074/jbc.272.32.20131 9242687
32. Yang G Nguyen X Ou J Rekulapelli P Stevenson DK Dennery PA Unique effects of zinc protoporphyrin on HO-1 induction and apoptosis Blood 2001, 97:1306-1313. 10.1182/blood.V97.5.1306 11222374
33. Sato K Ito K Kohara H Yamaguchi Y Adachi K Endo H Negative regulation of catalase gene expression in hepatoma cells Mol Cell Biol 1992, 12:2525-2533. 364445 1588955
34. Hasegawa Y Takano T Miyauchi A Matsuzuka F Yoshida H Kuma K Amino N Decreased expression of glutathione peroxidase mRNA in thyroid anaplastic carcinoma Cancer Lett 2002, 182:69-74. 10.1016/ S0304-3835(02)00069-1 12175525
35. Yamanaka N Deamer D Superoxide dismutase activity in WI-38 cell cultures: Effects of age, trypsinization and SV-40 transformation Physiol Chem Phys 1974, 6:95-106. 4369250
36. Farrera JA Jauma A Ribo JM Peire MA Parellada PP Roques-Choua S Bienvenue E Seta P The antioxidant role of bile pigments evaluated by chemical tests Bioorg Med Chem 1994, 2:181-185. 10.1016/ S0968-0896(00)82013-1 7922130
37. Minetti M Mallozzi C Di Stasi AM Pietraforte D Bilirubin is an effective antioxidant of peroxynitrite-mediated protein oxidation in human blood plasma Arch Biochem Biophys 1998, 352:165-174. 10.1006/abbi.1998.0584 9587403
38. Dore S Takahashi M Ferris CD Zakhary R Hester LD Guastella D Snyder SH Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury Proc Natl Acad Sci USA 1999, 96:2445-2450. 26804 10051662 10.1073/pnas.96.5.2445
39. Petrache I Otterbein LE Alam J Wiegand GW Choi AM Heme oxygenase-1 inhibits TNF-alpha-induced apoptosis in cultured fibroblasts Am J Physiol Lung Cell Mol Physiol 2000, 278:L312-319. 10666115
40. Otterbein LE Mantell LL Choi AM Carbon monoxide provides protection against hyperoxic lung injury Am J Physiol 1999, 276:L688-694. 10198367
41. Sato K Balla J Otterbein L Smith RN Brouard S Lin Y Csizmadia E Sevigny J Robson SC Vercellotti G et al. Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants J Immunol 2001, 166:4185-4194. 11238670
42. Lee TS Chau LY Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice Nat Med 2002, 8:240-246. 10.1038/nm0302-240 11875494
43. Richardson DR Molecular mechanisms of iron uptake by cells and the use of iron chelators for the treatment of cancer Curr Med Chem 2005, 12:2711-2729. 10.2174/092986705774462996 16305467
44. Darnell G Richardson DR The potential of iron chelators of the pyridoxal isonicotinoyl hydrazone class as effective antiproliferative agents III: the effect of the ligands on molecular targets involved in proliferation Blood 1999, 94:781-792. 10397746
45. Becton DL Roberts B Antileukemic effects of deferoxamine on human myeloid leukemia cell lines Cancer Res 1989, 49:4809-4812. 2758414
46. Brodie C Siriwardana G Lucas J Schleicher R Terada N Szepesi A Gelfand E Seligman P Neuroblastoma sensitivity to growth inhibition by deferrioxamine: Evidence for a block in G1 phase of the cell cycle Cancer Res 1993, 53:3968-3975. 8358725
47. Donfrancesco A Deb G Dominici C Pileggi D Castello MA Helson L Effects of a single course of deferoxamine in neuroblastoma patients Cancer Res 1990, 50:4929-4930. 2379156
48. Guo J Kleeff J Li J Ding J Hammer J Zhao Y Giese T Korc M Buchler MW Friess H Expression and functional significance of CDC25B in human pancreatic ductal adenocarcinoma Oncogene 2004, 23:71-81. 10.1038/ sj.onc.1206926 14712212
49. Kunzli BM Nuhn P Enjyoji K Banz Y Smith RN Csizmadia E Schuppan D Berberat PO Friess H Robson SC Disordered Pancreatic Inflammatory Responses and Inhibition of Fibrosis in CD39-Null Mice Gastroenterology 2008, 134(1):292-305. 2189558 18036594 10.1053/j.gastro.2007.10.030