A functional perspective of nitazoxanide as a potential anticancer drug

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 768, Issue C, 2014, Pages 16-21

  Di Santo, Nicola ^a   Ehrisman, Jessie ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Autophagy; c Myc; Glutathione S transferase; Interleukin 6; Microenvironment; Nitazoxanide; Protein disulfide isomerase

Indexed keywords

ANTINEOPLASTIC AGENT; ANTIPARASITIC AGENT; MYC PROTEIN; MYC PROTEIN, HUMAN; NITAZOXANIDE; THIAZOLE DERIVATIVE;

ANIMAL; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; HUMAN; METABOLISM; NEOPLASMS; PATHOLOGY; SIGNAL TRANSDUCTION; STROMA CELL; UNFOLDED PROTEIN RESPONSE;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTIPARASITIC AGENTS; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; STROMAL CELLS; THIAZOLES; UNFOLDED PROTEIN RESPONSE;

EID: 84929043287     PISSN: 00275107     EISSN: 18792871     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2014.05.005     Document Type: Review

References (78)

1. White A.C. Nitazoxanide: a new broad spectrum antiparasitic agent. Expert Rev. Anti Infect. Ther. 2004, 2:43-49.
2. Theodos C.M., Griffiths J.K., D'Onfro J., Fairfield A., Tzipori S. Efficacy of nitazoxanide against Cryptosporidium parvum in cell culture and in animal models. Antimicrob. Agents Chemother. 1998, 42:1959-1965.
3. Elazar M., Liu M., McKenna S.A., Liu P., Gehrig E.A., Puglisi J.D., Rossignol J.F., Glenn J.S. The anti-hepatitis C agent nitazoxanide induces phosphorylation of eukaryotic initiation factor 2α via protein kinase activated by double-stranded RNA activation. Gastroenterology 2009, 137:1827-1835.
4. Müller J., Naguleswaran A., Müller N., Hemphill A. Neospora caninum: functional inhibition of protein disulfide isomerase by the broad-spectrum anti-parasitic drug nitazoxanide and other thiazolides. Exp. Parasitol. 2008, 118:80-88.
5. Anderson V., Curran M. nitazoxanide. Drugs 2007, 67:1947-1967.
6. Müller J., Sidler D., Nachbur U., Wastling J., Brunner T., Hemphill A. Thiazolides inhibit growth and induce glutathione-S-transferase Pi (GSTP1)-dependent cell death in human colon cancer cells. Int. J. Cancer 2008, 123:1797-1806.
7. Fan-Minogue H., Bodapati S., Solow-Cordero D.E., Fan A., Paulmurugan R., Massoud T., Felsher D.W., Gambhir S.S. A c-Myc activation sensor-based high throughput drug screening identifies an anti-neoplastic effect of nitazoxanide. Mol. Cancer Ther. 2013, 12:1896-1905.
8. Gruber C.W., Čemažar M., Heras B., Martin J.L., Craik D.J. Protein disulfide isomerase: the structure of oxidative folding. Trends Biochem. Sci. 2006, 31:455-464.
9. Hebert D.N., Bernasconi R., Molinari M. ERAD substrates: which way out?. Semin. Cell Dev. Biol. 2010, 21:526-532.
10. Feldman D.E., Chauhan V., Koong A.C. The unfolded protein response: a novel component of the hypoxic stress response in tumors. Mol. Cancer Res. 2005, 3:597-605.
11. Welsh J.B., Sapinoso L.M., Su A.I., Kern S.G., Wang-Rodriguez J., Moskaluk C.A., Frierson H.F., Hampton G.M. Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res. 2001, 61:5974-5978.
12. Piccaluga P.P., Agostinelli C., Califano A., Rossi M., Basso K., Zupo S., Went P., Klein U., Zinzani P.L., Baccarani M., Dalla Favera R., Pileri S.A. Gene expression analysis of peripheral T cell lymphoma, unspecified, reveals distinct profiles and new potential therapeutic targets. J. Clin. Investig. 2007, 117:823-834.
13. Basso K., Margolin A.A., Stolovitzky G., Klein U., Dalla-Favera R., Califano A. Reverse engineering of regulatory networks in human B cells. Nat. Genet. 2005, 37:382-390.
14. Goplen D., Wang J., Enger P.Ø., Tysnes B.B., Terzis A.J.A., Laerum O.D., Bjerkvig R. Protein disulfide isomerase expression is related to the invasive properties of Malignant Glioma. Cancer Res. 2006, 66:9895-9902.
15. Bonome T., Levine D.A., Shih J., Randonovich M., Pise-Masison C.A., Bogomolniy F., Ozbun L., Brady J., Barrett J.C., Boyd J., Birrer M.J. A gene signature predicting for survival in suboptimally debulked patients with ovarian cancer. Cancer Res. 2008, 68:5478-5486.
16. Lovat P.E., Corazzari M., Armstrong J.L., Martin S., Pagliarini V., Hill D., Brown A.M., Piacentini M., Birch-Machin M.A., Redfern C.P.F. Increasing melanoma cell death using inhibitors of protein disulfide isomerases to abrogate survival responses to endoplasmic reticulum stress. Cancer Res. 2008, 68:5363-5369.
17. Xu S., Butkevich A.N., Yamada R., Zhou Y., Debnath B., Duncan R., Zandi E., Petasis N.A., Neamati N. Discovery of an orally active small-molecule irreversible inhibitor of protein disulfide isomerase for ovarian cancer treatment. Proc. Natl. Acad. Sci. 2012, 109:16348-16353.
18. Di Santo N., Ehrisman J. Research perspective potential role of nitazoxanide in ovarian cancer treatment. Old drug, new purpose?. Cancers 2013, 5:1163-1176.
19. Petty R., Evans A., Duncan I., Kurbacher C., Cree I. Drug resistance in ovarian cancer-the role of p53. Pathol. Oncol. Res. 1998, 4:97-102.
20. Havrilesky L., Darcy K.M., Hamdan H., Priore R.L., Leon J., Bell J., Berchuck A. Prognostic significance of p53 mutation and p53 overexpression in advanced epithelial ovarian cancer: a gynecologic oncology group study. J. Clin. Oncol. 2003, 21:3814-3825.
21. Konstantinova I.M., Tsimokha A.S., Mittenberg A.G. Role of proteasomes in cellular regulation. International Review of Cell and Molecular Biology 2008, 59-124. Academic Press, Waltham, Massachusetts. W.J. Kwang (Ed.).
22. McLean K., VanDeVen N.A., Sorenson D.R., Daudi S., Liu J.R. The HIV protease inhibitor saquinavir induces endoplasmic reticulum stress, autophagy, and apoptosis in ovarian cancer cells. Gynecol. Oncol. 2009, 112:623-630.
23. Klionsky D.J., Emr S.D. Autophagy as a regulated pathway of cellular degradation. Science 2000, 290:1717-1721.
24. Høyer-Hansen M., Jäättelä M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 2007, 14:1576-1582.
25. Debnath J., Baehrecke E.H., Kroemer G. Does autophagy contribute to cell death?. Autophagy 2005, 1:66-74.
26. Ogata M., Hino S.-I., Saito A., Morikawa K., Kondo S., Kanemoto S., Murakami T., Taniguchi M., Tanii I., Yoshinaga K. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell Biol. 2006, 26:9220-9231.
27. Reedijk J. Increased understanding of platinum anticancer chemistry. Pure Appl. Chem. 2011, 83:1709-1719.
28. Lyttle M.H., Satyam A., Hocker M.D., Bauer K.E., Caldwell C.G., Hui H.C., Morgan A.S., Mergia A., Kauvar L.M. Glutathione-S-transferase activates novel alkylating agents. J. Med. Chem. 1994, 37:1501-1507.
29. Gate L., Tew K. Alkylating agents. Cancer Management in Man: Chemotherapy, Biological Therapy, Hyperthermia and Supporting Measures 2011, 61-85. Springer, Netherlands. B.R. Minev (Ed.).
30. Adler V., Yin Z., Fuchs S.Y., Benezra M., Rosario L., Tew K.D., Pincus M.R., Sardana M., Henderson C.J., Wolf C.R. Regulation of JNK signaling by GSTp. EMBO J. 1999, 18:1321-1334.
31. Hayes J.D., Strange R.C. Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology 2000, 61:154-166.
32. Vergote I., Finkler N.J., Hall J.B., Melnyk O., Edwards R.P., Jones M., Keck J.G., Meng L., Brown G.L., Rankin E.M., Burke J.J., Boccia R.V., Runowicz C.D., Rose P.G. Randomized phase III study of canfosfamide in combination with pegylated liposomal doxorubicin compared with pegylated liposomal doxorubicin alone in platinum-resistant ovarian cancer. Int. J. Gynecol. Cancer 2010, 20:772-780. 10.1111/IGC.1110b1013e3181daaf1159.
33. Lam K.K., Zheng X., Forestieri R., Balgi A.D., Nodwell M., Vollett S., Anderson H.J., Andersen R.J., Av-Gay Y., Roberge M. Nitazoxanide stimulates autophagy and inhibits mTORC1 signaling and intracellular proliferation of Mycobacterium tuberculosis. PLoS Pathog. 2012, 8:e1002691.
34. Guertin D.A., Sabatini D.M. Defining the role of mTOR in cancer. Cancer Cell 2007, 12:9-22.
35. Ekstrand A., Jönsson M., Lindblom A., Borg Å., Nilbert M. Frequent alterations of the PI3K/AKT/mTOR pathways in hereditary nonpolyposis colorectal cancer. Fam. Cancer 2010, 9:125-129.
36. Haefliger S., Klebig C., Schaubitzer K., Schardt J., Timchenko N., Mueller B.U., Pabst T. Protein disulfide isomerase blocks CEBPA translation and is up-regulated during the unfolded protein response in AML. Blood 2011, 117:5931-5940.
37. Chan J.A., Zhang H., Roberts P.S., Jozwiak S., Wieslawa G., Lewin-Kowalik J., Kotulska K., Kwiatkowski D.J. Pathogenesis of tuberous sclerosis subependymal giant cell astrocytomas: biallelic inactivation of TSC1 or TSC2 leads to mTOR activation. J. Neuropathol. Exp. Neurol. 2004, 63:1236-1242.
38. Riemenschneider M.J., Betensky R.A., Pasedag S.M., Louis D.N. AKT activation in human glioblastomas enhances proliferation via TSC2 and S6 kinase signaling. Cancer Res. 2006, 66:5618-5623.
39. Altomare D.A., Wang H.Q., Skele K.L., De Rienzo A., Klein-Szanto A.J., Godwin A.K., Testa J.R. AKT and mTOR phosphorylation is frequently detected in ovarian cancer and can be targeted to disrupt ovarian tumor cell growth. Oncogene 2004, 23:5853-5857.
40. Chen Y.Q., Chen H.H., Rhoad A.E., Warner L., Caggiano T.J., Failli A., Zhang H.Z., Hsiao C.L., Nakanishi K., Molnarkimber K.L. A Putative sirolimus (rapamycin) effector protein. Biochem. Biophys. Res. Commun. 1994, 203:1-7.
41. Chan S., Scheulen M.E., Johnston S., Mross K., Cardoso F., Dittrich C., Eiermann W., Hess D., Morant R., Semiglazov V. Phase II study of temsirolimus (CCI-779), a novel inhibitor of mTOR, in heavily pretreated patients with locally advanced or metastatic breast cancer. J. Clin. Oncol. 2005, 23:5314-5322.
42. Duran I., Kortmansky J., Singh D., Hirte H., Kocha W., Goss G., Le L., Oza A., Nicklee T., Ho J. A phase II clinical and pharmacodynamic study of temsirolimus in advanced neuroendocrine carcinomas. Br. J. Cancer 2006, 95:1148-1154.
43. Galanis E., Buckner J.C., Maurer M.J., Kreisberg J.I., Ballman K., Boni J., Peralba J.M., Jenkins R.B., Dakhil S.R., Morton R.F. Phase II trial of temsirolimus (CCI-779) in recurrent glioblastoma multiforme: a North Central Cancer Treatment Group Study. J. Clin. Oncol. 2005, 23:5294-5304.
44. Levine B., Mizushima N., Virgin H.W. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
45. Ravikumar B., Sarkar S., Davies J.E., Futter M., Garcia-Arencibia M., Green-Thompson Z.W., Jimenez-Sanchez M., Korolchuk V.I., Lichtenberg M., Luo S. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev. 2010, 90:1383-1435.
46. Wang K., Klionsky D.J. Mitochondria removal by autophagy. Autophagy 2011, 7:297-300.
47. Colombo N., McMeekin S., Schwartz P., Kostka J., Sessa C., Gehrig P., Holloway R., Braly P., Matei D., Einstein M. A phase II trial of the mTOR inhibitor AP23573 as a single agent in advanced endometrial cancer. J. Clin. Oncol. 2007, 25(18 suppl). Abstract ID: 5516 (Meeting Abstracts).
48. Mackay H., Welch S., Tsao M.S., Biagi J.J., Elit L., Ghatage P., Martin L.A., Tonkin K.S., Ellard S., Lau S.K., McIntosh L., Eisenhauer E.A., Oza A.M. Phase II study of oral ridaforolimus in patients with metastatic and/or locally advanced recurrent endometrial cancer: NCIC CTG IND 192. J. Clin. Oncol. 2011, 29. (suppl; abstr 5013).
49. Behbakht K., Sill M.W., Darcy K.M., Rubin S.C., Mannel R.S., Waggoner S., Schilder R.J., Cai K.Q., Godwin A.K., Alpaugh R.K. Phase II trial of the mTOR inhibitor, temsirolimus and evaluation of circulating tumor cells and tumor biomarkers in persistent and recurrent epithelial ovarian and primary peritoneal malignancies: a Gynecologic Oncology Group study. Gynecol. Oncol. 2011, 123:19-26.
50. Jung C.H., Ro S.-H., Cao J., Otto N.M., Kim D.-H. mTOR regulation of autophagy. FEBS Lett. 2010, 584:1287-1295.
51. Mutter G.L., Lin M.-C., Fitzgerald J.T., Kum J.B., Baak J.P., Lees J.A., Weng L.-P., Eng C., Altered P.T.E.N. expression as a diagnostic marker for the earliest endometrial precancers. J. Natl. Cancer Inst. 2000, 92:924-930.
52. Djordjevic B., Hennessy B.T., Li J., Barkoh B.A., Luthra R., Mills G.B., Broaddus R.R. Clinical assessment of PTEN loss in endometrial carcinoma: immunohistochemistry outperforms gene sequencing. Mod. Pathol. 2012, 25:699-708.
53. Chang Y.-Y., Neufeld T.P. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol. Biol. Cell 2009, 20:2004-2014.
54. Aita V.M., Liang X.H., Murty V.V.V.S., Pincus D.L., Yu W., Cayanis E., Kalachikov S., Gilliam T.C., Levine B. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 1999, 59:59-65.
55. Amaravadi R.K., Lippincott-Schwartz J., Yin X.-M., Weiss W.A., Takebe N., Timmer W., DiPaola R.S., Lotze M.T., White E. Principles and current strategies for targeting autophagy for cancer treatment. Clin. Cancer Res. 2011, 17:654-666.
56. Lakhter A.J., Sahu R.P., Sun Y., Kaufmann W.K., Androphy E.J., Travers J.B., Naidu S.R. Chloroquine promotes apoptosis in melanoma cells by inhibiting BH3 domain-mediated PUMA degradation. J. Invest. Dermatol. 2013, 133:2247-2254.
57. Bursch W., Ellinger A., Kienzl H., Török L., Pandey S., Sikorska M., Walker R., Hermann R.S. Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis 1996, 17:1595-1607.
58. Martinez-Outschoorn U.E., Balliet R.M., Rivadeneira D.B., Chiavarina B., Pavlides S., Wang C., Whitaker-Menezes D., Daumer K.M., Lin Z., Witkiewicz A.K. Oxidative stress in cancer associated fibroblasts drives tumor-stroma co-evolution: a new paradigm for understanding tumor metabolism, the field effect and genomic instability in cancer cells. Cell Cycle 2010, 9:3256.
59. Martinez-Outschoorn U.E., Pavlides S., Howell A., Pestell R.G., Tanowitz H.B., Sotgia F., Lisanti M.P. Stromal-epithelial metabolic coupling in cancer: integrating autophagy and metabolism in the tumor microenvironment. Int. J. Biochem. Cell Biol. 2011, 43:1045-1051.
60. Tlsty T.D., Coussens L.M. Tumor stroma and regulation of cancer development. Annu. Rev. Pathol. Mech. Dis. 2006, 1:119-150.
61. Amati B., Alevizopoulos K., Vlach J. Myc and the cell cycle. Front. Biosci. 1998, 3:d250-d268.
62. Herold S., Herkert B., Eilers M. Facilitating replication under stress: an oncogenic function of MYC?. Nat. Rev. Cancer 2009, 9:441-444.
63. Dang C.V., Le A., Gao P. MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clin. Cancer Res. 2009, 15:6479-6483.
64. Maes H., Rubio N., Garg A.D., Agostinis P. Autophagy: shaping the tumor microenvironment and therapeutic response. Trends Mol. Med. 2013, 19:428-446.
65. Hurst S.M., Wilkinson T.S., McLoughlin R.M., Jones S., Horiuchi S., Yamamoto N., Rose-John S., Fuller G.M., Topley N., Jones S.A. IL-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 2001, 14:705-714.
66. Wei L.-H., Kuo M.-L., Chen C.-A., Chou C.-H., Lai K.-B., Lee C.-N., Hsieh C.-Y. Interleukin-6 promotes cervical tumor growth by VEGF-dependent angiogenesis via a STAT3 pathway. Oncogene 2003, 22:1517-1527.
67. Coward J.I., Kulbe H. The role of interleukin-6 in gynaecological malignancies. Cytokine Growth Factor Rev. 2012, 23:333-342.
68. Sansone P., Storci G., Tavolari S., Guarnieri T., Giovannini C., Taffurelli M., Ceccarelli C., Santini D., Paterini P., Marcu K.B. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J. Clin. Invest. 2007, 117:3988-4002.
69. Culig Z., Bartsch G., Hobisch A. Interleukin-6 regulates androgen receptor activity and prostate cancer cell growth. Mol. Cell. Endocrinol. 2002, 197:231-238.
70. Feurino L.W., Zhang Y., Bharadwaj U., Zhang R., Li F., Fisher W.E., Brunicardi F.C., Chen C., Yao Q., Li M. IL-6 stimulates Th2 type cytokine secretion and upregulates VEGF and NRP-1 expression in pancreatic cancer cells. Cancer Biol. Ther. 2007, 6:1096.
71. Holzinger C., Weissinger E., Zuckermann A., Imhof M., Kink F., Schöllhammer A., Kopp C., Wolner E. Effects of interleukin-1, -2, -4, -6, interferon-gamma and granulocyte/macrophage colony stimulating factor on human vascular endothelial cells. Immunol. Lett. 1993, 35:109-117.
72. Saidi A., Hagedorn M., Allain N., Verpelli C., Sala C., Bello L., Bikfalvi A., Javerzat S. Combined targeting of interleukin-6 and vascular endothelial growth factor potently inhibits glioma growth and invasiveness. Int. J. Cancer 2009, 125:1054-1064.
73. Hong S.K., Kim H.J., Song C.S., Choi I.S., Lee J.B., Park S.Y. Nitazoxanide suppresses IL-6 production in LPS-stimulated mouse macrophages and TG-injected mice. Int. Immunopharmacol. 2012, 13:23-27.
74. Jiang H., Wek R. GCN2 phosphorylation of eIF2alpha activates NF-kappaB in response to UV irradiation. Biochem. J. 2005, 385:371-380.
75. Karin M., Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 2000, 18:621-663.
76. Courtois G., Gilmore T. Mutations in the NF-κB signaling pathway: implications for human disease. Oncogene 2006, 25:6831-6843.
77. Zimmermann G.R., Lehár J., Keith C.T. Multi-target therapeutics: when the whole is greater than the sum of the parts. Drug Discov. Today 2007, 12:34-42.
78. Raju T.N.K. The nobel chronicles. Lancet 2000, 355:1022.