Targeting cancer stem cells expressing an embryonic signature with anti-proteases to decrease their tumor potential

Cell Death and Disease

Volumn 4, Issue 7, 2013, Pages

  Darini, C Y ^a,b,f,g   Martin, P ^a,b,f   Azoulay, S ^c   Drici, M D ^d   Hofman, P ^e   Obba, S ^a,b   Dani, C ^a,b   Ladoux, A ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c UNIVERSITÉ DE NICE SOPHIA ANTIPOLIS   (France)

^d UNIVERSITY HOSPITAL OF NICE   (France)

^e INSERM   (France)

^f CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^g CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

Author keywords

Apoptosis; Cancer stem cells; HIV protease inhibitors; Oct 4; Stemness signature

Indexed keywords

AMPRENAVIR; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR; INDINAVIR; LOPINAVIR; NELFINAVIR; OCTAMER TRANSCRIPTION FACTOR 4; RITONAVIR; SALINOMYCIN; SAQUINAVIR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER STEM CELL; CELL PROLIFERATION; CONTROLLED STUDY; DRUG TARGETING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 84881065135     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.206     Document Type: Article

References (56)

1. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66: 9339-9344.
2. Sleeman J, Steeg PS. Cancer metastasis as a therapeutic target. Eur J Cancer 2010; 46: 1177-1180.
3. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007; 11: 259-273.
4. Sugihara E, Saya H. Complexity of cancer stem cells. Int J Cancer 2012; 132: 1249-1259.
5. Valent P, Bonnet D, De Maria R, Lapidot T, Copland M, Melo JV et al. Cancer stem cell definitions and terminology: the devil is in the details. Nat Rev Cancer 2012; 12: 767-775.
6. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988.
7. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V et al. Identification of pancreatic cancer stem cells. Cancer Res 2007; 67: 1030-1037.
8. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007; 445: 111-115.
9. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T et al. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401.
10. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007; 1: 555-567.
11. Kondo T, Setoguchi T, Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA 2004; 101: 781-786.
12. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
13. Baccelli I, Trumpp A. The evolving concept of cancer and metastasis stem cells. J Cell Biol 2012; 198: 281-293.
14. Darini CY, Pisani DF, Hofman P, Pedeutour F, Sudaka I, Chomienne C et al. Self-renewal gene tracking to identify tumour-initiating cells associated with metastatic potential. Oncogene 2012; 31: 2438-2449.
15. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40: 499-507.
16. Chiou SH, Wang ML, Chou YT, Chen CJ, Hong CF, Hsieh WJ et al. Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem celllike properties and epithelial-mesenchymal transdifferentiation. Cancer Res 2010; 70: 10433-10444.
17. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 2007; 17: 165-172.
18. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-760.
19. Dean M. Cancer stem cells: implications for cancer causation and therapy resistance. Discov Med 2005; 5: 278-282.
20. Diehn M, Cho RW, Clarke MF. Therapeutic implications of the cancer stem cell hypothesis. Semin Radiat Oncol 2009; 19: 78-86.
21. Diehn M, Clarke MF. Cancer stem cells and radiotherapy: new insights into tumor radioresistance. J Natl Cancer Inst 2006; 98: 1755-1757.
22. Eyler CE, Rich JN. Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol 2008; 26: 2839-2845.
23. Woodward WA, Chen MS, Behbod F, Alfaro MP, Buchholz TA, Rosen JM. WNT/betacatenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci USA 2007; 104: 618-623.
24. Gavrilov K, Saltzman WM. Therapeutic siRNA: principles, challenges, and strategies. Yale J Biol Med 2012; 85: 187-200.
25. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 2006; 12: 1167-1174.
26. Marangoni E, Lecomte N, Durand L, de Pinieux G, Decaudin D, Chomienne C et al. CD44 targeting reduces tumour growth and prevents post-chemotherapy relapse of human breast cancers xenografts. Br J Cancer 2009; 100: 918-922.
27. Autran B, Carcelaint G, Li TS, Gorochov G, Blanc C, Renaud M et al. Restoration of the immune system with anti-retroviral therapy. Immunol Lett 1999; 66: 207-211.
28. Vella S, Palmisano L. Antiretroviral therapy: state of the HAART. Antiviral Res 2000; 45: 1-7.
29. Gill J, Bourboulia D, Wilkinson J, Hayes P, Cope A, Marcelin AG et al. Prospective study of the effects of antiretroviral therapy on Kaposi sarcoma-associated herpesvirus infection in patients with and without Kaposi sarcoma. J Acquir Immune Defic Syndr 2002; 31: 384-390.
30. Monini P, Sgadari C, Grosso MG, Bellino S, Di Biagio A, Toschi E et al. Clinical course of classic Kaposi's sarcoma in HIV-negative patients treated with the HIV protease inhibitor indinavir. Aids 2009; 23: 534-538.
31. McLean K, VanDeVen NA, Sorenson DR, Daudi S, Liu JR. The HIV protease inhibitor saquinavir induces endoplasmic reticulum stress, autophagy, and apoptosis in ovarian cancer cells. Gynecol Oncol 2009; 112: 623-630.
32. Pyrko P, Kardosh A, Wang W, Xiong W, Schonthal AH, Chen TC. HIV-1 protease inhibitors nelfinavir and atazanavir induce malignant glioma death by triggering endoplasmic reticulum stress. Cancer Res 2007; 67: 10920-10928.
33. Yang Y, Ikezoe T, Takeuchi T, Adachi Y, Ohtsuki Y, Takeuchi S et al. HIV-1 protease inhibitor induces growth arrest and apoptosis of human prostate cancer LNCaP cells in vitro and in vivo in conjunction with blockade of androgen receptor STAT3 and AKT signaling. Cancer Sci 2005; 96: 425-433.
34. Esposito V, Palescandolo E, Spugnini EP, Montesarchio V, De Luca A, Cardillo I et al. Evaluation of antitumoral properties of the protease inhibitor indinavir in a murine model of hepatocarcinoma. Clin Cancer Res 2006; 12: 2634-2639.
35. Chaitanya GV, Steven AJ, Babu PP. PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration. Cell Commun Signal 2010; 8: 31.
36. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009; 138: 645-659.
37. Prot M, Heripret L, Cardot-Leccia N, Perrin C, Aouadi M, Lavrut T et al. Long-term treatment with lopinavir-ritonavir induces a reduction in peripheral adipose depots in mice. Antimicrob Agents Chemother 2006; 50: 3998-4004.
38. Magee JA, Piskounova E, Morrison SJ. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell 2012; 21: 283-296.
39. Monini P, Sgadari C, Toschi E, Barillari G, Ensoli B. Antitumour effects of antiretroviral therapy. Nat Rev Cancer 2004; 4: 861-875.
40. Ikezoe T, Saito T, Bandobashi K, Yang Y, Koeffler HP, Taguchi H. HIV-1 protease inhibitor induces growth arrest and apoptosis of human multiple myeloma cells via inactivation of signal transducer and activator of transcription 3 and extracellular signal-regulated kinase 1/2. Mol Cancer Ther 2004; 3: 473-479.
41. Gills JJ, Lopiccolo J, Tsurutani J, Shoemaker RH, Best CJ, Abu-Asab MS et al. Nelfinavir, a lead HIV protease inhibitor, is a broad-spectrum, anticancer agent that induces endoplasmic reticulum stress, autophagy, and apoptosis in vitro and in vivo. Clin Cancer Res 2007; 13: 5183-5194.
42. Johnson MD, O'Connell M, Pilcher W. Lopinavir inhibits meningioma cell proliferation by Akt independent mechanism. J Neurooncol 2011; 101: 441-448.
43. Sachlos E, Risueno RM, Laronde S, Shapovalova Z, Lee JH, Russell J et al. Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell 2012; 149: 1284-1297.
44. Dash C, Kulkarni A, Dunn B, Rao M. Aspartic peptidase inhibitors: implications in drug development. Crit Rev Biochem Mol Biol 2003; 38: 89-119.
45. Benes P, Vetvicka V, Fusek M. Cathepsin D-many functions of one aspartic protease. Crit Rev Oncol Hematol 2008; 68: 12-28.
46. Sham HL, Zhao C, Li L, Betebenner DA, Saldivar A, Vasavanonda S et al. Novel lopinavir analogues incorporating non-aromatic P-1 side chains-synthesis and structure-activity relationships. Bioorg Med Chem Lett 2002; 12: 3101-3103.
47. Sham HL, Kempf DJ, Molla A, Marsh KC, Kumar GN, Chen CM et al. ABT-378, a highly potent inhibitor of the human immunodeficiency virus protease. Antimicrob Agents Chemother 1998; 42: 3218-3224.
48. Djedaini M, Peraldi P, Drici MD, Darini C, Saint-Marc P, Dani C et al. Lopinavir co-induces insulin resistance and ER stress in human adipocytes. Biochem Biophys Res Commun 2009; 386: 96-100.
49. Caron-Debarle M, Boccara F, Lagathu C, Antoine B, Cervera P, Bastard JP et al. Adipose tissue as a target of HIV-1 antiretroviral drugs. Potential consequences on metabolic regulations. Curr Pharm Des 2010; 16: 3352-3360.
50. Vernochet C, Azoulay S, Duval D, Guedj R, Cottrez F, Vidal H et al. Human immunodeficiency virus protease inhibitors accumulate into cultured human adipocytes and alter expression of adipocytokines. J Biol Chem 2005; 280: 2238-2243.
51. Caron M, Auclair M, Lagathu C, Lombes A, Walker UA, Kornprobst M et al. The HIV-1 nucleoside reverse transcriptase inhibitors stavudine and zidovudine alter adipocyte functions in vitro. Aids 2004; 18: 2127-2136.
52. Zhang S, Carper MJ, Lei X, Cade WT, Yarasheski KE, Ramanadham S. Protease inhibitors used in the treatment of HIV\+ induce beta-cell apoptosis via the mitochondrial pathway and compromise insulin secretion. Am J Physiol Endocrinol Metab 2009; 296: E925-E935.
53. Stoner EJ, Cooper AJ, Dickman DA, Kolaczkowski L, Lallaman JE, Liu JH et al. Synthesis of HIV Protease Inhibitor ABT-378 (Lopinavir). Org Process Res Dev 2000; 4: 264-269.
54. Wdziekonski B, Villageois P, Dani C. Development of adipocytes from differentiated ES cells. Methods Enzymol 2003; 365: 268-277.
55. Rodriguez AM, Pisani D, Dechesne CA, Turc-Carel C, Kurzenne JY, Wdziekonski B et al. Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med 2005; 201: 1397-1405.
56. Thuerauf DJ, Marcinko M, Gude N, Rubio M, Sussman MA, Glembotski CC. Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ Res 2006; 99: 275-282.