Inhibition of Lon blocks cell proliferation, enhances chemosensitivity by promoting apoptosis and decreases cellular bioenergetics of bladder cancer: Potential roles of Lon as a prognostic marker and therapeutic target in baldder cancer

Oncotarget

Volumn 5, Issue 22, 2014, Pages 11209-11224

  Liu, Yongzhang ^a   Lan, Linhua ^a   Huang, Kate ^b   Wang, Rongrong ^b   Xu, Cuicui ^a   Shi, Yang ^a   Wu, Xiaoyi ^a   Wu, Zhi ^a   Zhang, Jiliang ^a   Chen, Lin ^a   Wang, Lu ^a   Yu, Xiaomin ^a   Zhu, Haibo ^c   Lu, Bin ^a  

^a WENZHOU MEDICAL UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF WENZHOU MEDICAL UNIVERSITY   (China)

^c THE SECOND AFFILIATED HOSPITAL AND YUYING CHILDREN S HOSPITAL OF WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Bladder cancer; Cellular bioenergetics; Chemosensitivity; Lon protease; Mitochondria; Protein quality control

Indexed keywords

CASPASE; ENDOPEPTIDASE LA; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; ANTIMYCIN A1; MESSENGER RNA; PROTEINASE INHIBITOR; TUMOR MARKER;

AEROBIC METABOLISM; AGED; APOPTOSIS; ARTICLE; BLADDER CANCER; BLADDER CANCER CELL LINE; CANCER PROGNOSIS; CANCER STAGING; CANCER TISSUE; CELL ENERGY; CELL PROLIFERATION; CHEMOSENSITIVITY; CONTROLLED STUDY; CORRELATIONAL STUDY; DOWN REGULATION; ENZYME ACTIVATION; FEMALE; GLYCOLYSIS; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MITOCHONDRIAL RESPIRATION; OVERALL SURVIVAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TISSUE MICROARRAY; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG EFFECTS; ENERGY METABOLISM; ENZYMOLOGY; GENE SILENCING; GENETICS; METABOLISM; MITOCHONDRION; MOLECULARLY TARGETED THERAPY; PATHOLOGY; TUMOR CELL LINE; URINARY BLADDER NEOPLASMS;

AGED; ANTIMYCIN A; APOPTOSIS; BIOMARKERS, TUMOR; CELL LINE, TUMOR; CELL PROLIFERATION; DOWN-REGULATION; ENERGY METABOLISM; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MITOCHONDRIA; MOLECULAR TARGETED THERAPY; PROTEASE INHIBITORS; PROTEASE LA; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; URINARY BLADDER NEOPLASMS;

EID: 84917706645     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2026     Document Type: Article

References (45)

1. Venkatesh S, Lee J, Singh K, Lee I, Suzuki CK. Multitasking in the mitochondrion by the ATPdependent Lon protease. Biochim Biophys Acta. 2012; 1823(1):56-66.
2. Lee I, Suzuki CK. Functional mechanics of the ATPdependent Lon protease- lessons from endogenous protein and synthetic peptide substrates. Biochim Biophys Acta. 2008; 178(5):727-735.
3. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010; 60(5): 277-300.
4. Clavel J, Cordier S, Boccon-Gibod L, Hemon D. Tobacco and bladder cancer in males: increased risk for inhalers and smokers of black tobacco. Int J Cancer. 1989; 44(4): 605- 610.
5. Botteman MF, Pashos CL, Redaelli A, Laskin B, Hauser R. The health economics of bladder cancer: a comprehensive review of the published literature. Pharmacoeconomics. 2003; 21(18):1315-1330.
6. Avritscher EB, Cooksley CD, Grossman HB, Sabichi AL, Hamblin L, Dinney CP, Elting LS. Clinical model of lifetime cost of treating bladder cancer and associated complications. Urology. 2006; 68(3):549-553.
7. Dey P. Urinary markers of bladder carcinoma. Clin Chim Acta. 2004; 340(1-2):57-65.
8. Tsilibaris V, Maenhaut-Michel G, Van Melderen L. Biological roles of the Lon ATP-dependent protease. Res Microbiol. 2006; 157(8):701-713.
9. Lee I and Suzuki CK. Functional mechanics of the ATPdependent Lon protease- lessons from endogenous protein and synthetic peptide substrates. Biochim Biophys Acta. 2008; 1784(5): 727-735.
10. Bogenhagen DF, Rousseau D, Burke S. The layered structure of human mitochondrial DNA nucleoids. J Biol Chem. 2008; 283(6):3665-75.
11. Lu B, Liu T, Crosby JA, Thomas-Wohlever J, Lee I, Suzuki CK. The ATP-dependent Lon protease of Mus musculus is a DNA-binding protein that is functionally conserved between yeast and mammals. Gene. 2003; 306:45-55.
12. Pinti M, Gibellini L, De Biasi S, Nasi M, Roat E, O'Connor JE, Cossarizza A. Functional characterization of the promoter of the human Lon protease gene. Mitochondrion. 2011; 11(1):200-6.
13. Fu GK, Markovitz DM. The human LON protease binds to mitochondrial promoters in a single-stranded, site-specific, strand-specific manner. Biochemistry. 1998; 37(7):1905-9.
14. Liu T, Lu B, Lee I, Ondrovicova G, Kutejova E, Suzuki CK. DNA and RNA binding by the mitochondrial lon protease is regulated by nucleotide and protein substrate. J Biol Chem. 2004; 279(14):13902-10.
15. Bota DA, Davies KJ. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat Cell Biol. 2002; 4(9):674-680.
16. Granot Z, Kobiler O, Melamed-Book N, Eimerl S, Bahat A, Lu B, Braun S, Maurizi MR, Suzuki CK, Oppenheim AB, Orly J. Turnover of mitochondrial steroidogenic acute regulatory (StAR) protein by Lon protease: the unexpected effect of proteasome inhibitors. Mol Endocrinol. 2007; 21(9): 2164-2177.
17. Fukuda R, Zhang H, Kim JW, Shimoda L, DangCV, Semenza GL. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell. 2007; 129(1): 111-122.
18. Hori O, Ichinoda F, Tamatani T, Tamatani T, Yamaguchi A, Sato N, Ozawa K, Kitao Y, Miyazaki M, Harding HP, Ron D, Tohyama M, Stern DM, Ogawa S. Transmission of cell stress from endoplasmic reticulum to mitochondria: enhanced expression of Lon protease. J Cell Biol. 2002; 157(7): 1151-1160.
19. Goard CA, Schimmer AD. Mitochondrial matrix proteases as novel therapeutic targets in malignancy. Oncogene. 2013; doi:10.1038/onc.2013.228
20. Bulteau A, Bayot A. Mitochondrial protease and cancer. Biochim. Biophys.Acta. 2011; 1807:595-601.
21. Bota DA, Ngo JK, Davies KJ. Down-regulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radic Biol Med. 2005; 38(5):665-677.
22. Bernstein SH, VenkateshS, LiM, Lee J, Lu B, Hilchey S, Morse KM, Metcalfe HM, Andreeff M, Brookes PS, Suzuki CK. The mitochondrial ATP-dependent Lon protease: a novel target in lymphoma death mediated by the synthetic triterpenoid CDDO and its derivatives. Blood. 2012; 119(14):3321-3329.
23. Xue X, Zhu YF, Mao JP. Effect of RNA interference for Lon gene silencing on growth and apoptosis of human breast cancer MCF7 cells. Nan Fang Yi Ke Da Xue Xue Bao. 2007; 27(6):870-874.
24. Wang HM, Cheng KC, Lin CJ, Hsu SW, Fang WC, Hsu TF, Chiu CC, Chang HW, Hsu CH, Lee YL. Obtusilactone A and (-)-sesamin induce apoptosis in human lung cancer cells by inhibiting mitochondrial Lon protease and activating DNA damage checkpoints. Cancer Sci 2010; 101(12): 2612-2620.
25. Zhao Y, Wang ZB, Xu JX. Effect of cytochrome c on the generation and elimination of O2*- and H2O2 in mitochondria. J Biol Chem. 2003; 278(4):2356-60.
26. Kim EK, Choi EJ. Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta. 2010;1802(4):396-405.
27. Luciakova K, Sokolikova B, Chloupkova M, Nelson BD. Enhanced mitochondrial biogenesis is associated with increased expression of the mitochondrial ATP-dependent Lon protease. FEBS Lett. 1999; 444(2-3): 186-188.
28. Cheng C-W, Kuo C-Y, Fan C-C, Fang W-C, Jiang SS, Lo Y-K, Wang T-Y, Kao M-C, Lee AY-L. Overexpression of Lon contributes to survival and aggressive phenotype of cancer cells through mitochondrial complex I-mediated generation of reactive oxygen species. Cell death and disease. 2013; 4: e681. doi:10.1038/cddis.2013.204
29. Lu B, Lee J, Nie XB, Li M, Morozov YI, Venkatesh S, Bogenhagen DF, Temiakov D, Suzuki CK. Phosphorylation of human TFAM in mitochondria impairs DNA binding and promotes degradation by the AAA+ Lon protease. Molecular Cell. 2013; 49(1):121-32.
30. Qin ZK, Yang JA, Ye YL, Zhang X, Xu LH, Zhou FJ, Han H, Liu ZW, Song LB, MS Zeng. Expression of Bmi-1 is a prognostic marker in bladder cancer. BMC Cancer. 2009; 9:61.
31. Raitanen MP, Marttila T, Kaasinen E, Rintala E, Aine R, Tammela TL. Sensitivity of human complement factor H related protein (BTA stat) test and voided urine cytology in the diagnosis of bladder cancer. J Urol. 2000;163(6):1689- 1692.
32. Budman LI, Kassouf W, Steinberg JR. Biomarkers for detection and surveillance of bladder cancer. Can Urol Assoc J. 2008; 2(3):212-221.
33. Nie XB, Li M, Lu B, Zhang YX, Lan LH, Chen L and Lu JX. Down-regulating overexpressed human Lon in cervical cancer suppresses cell proliferation and bioenergetics. PLOS ONE. 2013; 8(11):1-9.
34. Ngo JK, Pomatto LC, Bota DA, Koop AL, Davies KJ. Impairment of Lon-Induced Protection Against the Accumulation of Oxidized Proteins in Senescent Wi-Fibroblasts. J Gerontol A Biol Sci Med Sci. 2011; 66A(11):1178-1185.
35. Ngo JK, Pomatto LC, Davies KJ. Upregulation of the mitochondrial Lon Protease allows adaptation to acute oxidative stress but dysregulation is associated with chronic stress, disease, and aging. Redox Biol. 2013;1(1):258-264.
36. Pinti M, Gibellini L, Guaraldi G, Orlando G, Gant TW, Morselli E, Nasi M, Salomoni P, Mussini C, Cossarizza A. Upregulation of nuclear-encoded mitochondrial LON protease in HAART-treated HIV-positive patients with lipodystrophy: implications for the pathogenesis of the disease. AIDS. 2010; 24(6):841-850.
37. Erjavec N, Bayot A, Gareil M, Camougrand N, Nystrom T, Friguet B, Bulteau AL. Deletion of the mitochondrial Pim1/Lon protease in yeast results in accelerated aging and impairment of the proteasome. Free Radic Biol Med. 2013; 56: 9-16.
38. Dai C, Whitesell L, Rogers AB, Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell. 2007; 130(6):1005-1018.
39. Leu JI, Pimkina J, Frank A, Murphy ME, George DL. A small molecule inhibitor of inducible heat shock protein 70. Mol Cell. 2009; 36(1):15-27.
40. Trepel J, Mollapour M, Giaccone G, Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer. 2010; 10(8):537-549.
41. Nocito A, Bubendorf L, Tinner EM, Süess K, Wagner U, Forster T, Kononen J, Fijan A, Bruderer J, Schmid U, Ackermann D, Maurer R, Alund G, Knönagel H, Rist M, Anabitarte M, et al. Microarrays of bladder cancer tissue are highly representative of proliferation index and histological grade. J. Pathol. 2001; 194(3): 349-357.
42. Wang CJ, Zhou ZG, Holmqvist A, Zhang H, Li Y, Adell G, Sun XF. Survivin expression quantified by Image Pro-Plus compared with visual assessment. Applied immunohistochemistry & molecular morphology: AIMM / official publication of the Society for Applied Immunohistochemistry. 2009; 17(6):530-535.
43. Remmele W, Stegner HE. Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ERICA) in breast cancer tissue. Pathologe. 1987; 8: 138-140.
44. Cheng AN, Jiang SS, Fan CC, Lo YK, Kuo CY, Chen CH, Liu YL, Lee CC, Chen WS, Huang TS, Wang TY, Lee AY . Increased Cdc7 expression is a marker of oral squamous cell carcinoma and overexpression of Cdc7 contributes to the resistance to DNA-damaging agents. Cancer letters. 2013; 337: 218-225.
45. Bolander Å, Agnarsdóttir M, Strömberg S, Ponten F, Hesselius P, Mathias Uhlenand M, Bergqvist M.The protein expression of TRP-1 and galectin-1 in cutaneous malignant melanomas. Cancer genomics & proteomics. 2008; 5: 293- 300.