Chitosan nanoparticle-mediated delivery of miRNA-34a decreases prostate tumor growth in the bone and its expression induces non-canonical autophagy

Oncotarget

Volumn 6, Issue 30, 2015, Pages 29161-29177

  Gaur, Sanchaika ^a,b,e   Wen, Yunfei ^a   Song, Jian H ^a   Parikh, Nila U ^a   Mangala, Lingegowda S ^a   Blessing, Alicia M ^c   Ivan, Cristina ^a   Wu, Sherry Y ^a   Varkaris, Andreas ^a   Shi, Yan ^c   Lopez Berestein, Gabriel ^a   Frigo, Daniel E ^c,d   Sood, Anil K ^a,b   Gallick, Gary E ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c University of Houston   (United States)

^d HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^e CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Autophagy; Bone metastasis; MiR 34a; Prostate cancer

Indexed keywords

AUTOPHAGY PROTEIN 4; AUTOPHAGY PROTEIN 5; AUTOPHAGY PROTEIN 7; BECLIN 1; CELL PROTEIN; CHITOSAN NANOPARTICLE; MICRORNA 34A; MYC PROTEIN; PROTEIN AXL; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; CHITOSAN; MICRORNA; MIRN34 MICRORNA, HUMAN; NANOPARTICLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BONE METASTASIS; CANCER INHIBITION; CELL CYCLE ARREST; CONTROLLED STUDY; DOWN REGULATION; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENE FUNCTION; HISTOPATHOLOGY; HUMAN; MOUSE; NON-CANONICAL AUTOPHAGY; NONHUMAN; PROSTATE TUMOR; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR GROWTH; ANIMAL; BONE NEOPLASMS; CELL PROLIFERATION; CHEMISTRY; DRUG SCREENING; GENE EXPRESSION REGULATION; GENE THERAPY; GENE TRANSFER; GENETIC TRANSFECTION; GENETICS; MALE; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; NUDE MOUSE; PATHOLOGY; PROCEDURES; PROSTATIC NEOPLASMS; RNA INTERFERENCE; SECONDARY; TIME FACTOR; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; APOPTOSIS; AUTOPHAGY; BONE NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CHITOSAN; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HUMANS; MALE; MICE, NUDE; MICRORNAS; NANOPARTICLES; PROSTATIC NEOPLASMS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TUMOR BURDEN; X-RAY MICROTOMOGRAPHY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84945152138     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4971     Document Type: Article

References (57)

1. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA: a cancer journal for clinicians. 2014; 64:9-29.
2. Lee RJ and Smith MR. Targeting MET and vascular endothelial growth factor receptor signaling in castration-resistant prostate cancer. Cancer J. 2013; 19:90-98.
3. Dayyani F, Gallick GE, Logothetis CJ and Corn PG. Novel therapies for metastatic castrate-resistant prostate cancer. Journal of the National Cancer Institute. 2011; 103:1665-1675.
4. Thoreson GR, Gayed BA, Chung PH and Raj GV. Emerging therapies in castration resistant prostate cancer. The Canadian journal of urology. 2014; 21:98-105.
5. Logothetis CJ, Gallick GE, Maity SN, Kim J, Aparicio A, Efstathiou E and Lin SH. Molecular classification of prostate cancer progression: foundation for marker-driven treatment of prostate cancer. Cancer Discov. 2013; 3:849-861.
6. Bader AG, Brown D and Winkler M. The promise of microRNA replacement therapy. Cancer research. 2010; 70:7027-7030.
7. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116:281-297.
8. Suzuki HI, Katsura A, Matsuyama H and Miyazono K. MicroRNA regulons in tumor microenvironment. Oncogene. 2014.
9. Tong AW and Nemunaitis J. Modulation of miRNA activity in human cancer: a new paradigm for cancer gene therapy? Cancer gene therapy. 2008; 15:341-355.
10. Daige CL, Wiggins JF, Priddy L, Nelligan-Davis T, Zhao J and Brown D. Systemic delivery of a miR-34a mimic as a potential therapeutic for liver cancer. Molecular cancer therapeutics. 2014.
11. Ibrahim AF, Weirauch U, Thomas M, Grunweller A, Hartmann RK and Aigner A. MicroRNA replacement therapy for miR-145 and miR-33a is efficacious in a model of colon carcinoma. Cancer research. 2011; 71:5214-5224.
12. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D and Tang DG. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nature medicine. 2011; 17:211-215.
13. Trang P, Wiggins JF, Daige CL, Cho C, Omotola M, Brown D, Weidhaas JB, Bader AG and Slack FJ. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Molecular therapy: the journal of the American Society of Gene Therapy. 2011; 19:1116-1122.
14. Mudduluru G, Ceppi P, Kumarswamy R, Scagliotti GV, Papotti M and Allgayer H. Regulation of Axl receptor tyrosine kinase expression by miR-34a and miR-199a/b in solid cancer. Oncogene. 2011; 30:2888-2899.
15. Yamamura S, Saini S, Majid S, Hirata H, Ueno K, Deng G and Dahiya R. MicroRNA-34a modulates c-Myc transcriptional complexes to suppress malignancy in human prostate cancer cells. PloS one. 2012; 7:e29722.
16. Krzeszinski JY, Wei W, Huynh H, Jin Z, Wang X, Chang TC, Xie XJ, He L, Mangala LS, Lopez-Berestein G, Sood AK, Mendell JT and Wan Y. miR-34a blocks osteoporosis and bone metastasis by inhibiting osteoclastogenesis and Tgif2. Nature. 2014.
17. Wen Y, Zand B, Ozpolat B, Szczepanski MJ, Lu C, Yuca E, Carroll AR, Alpay N, Bartholomeusz C, Tekedereli I, Kang Y, Rupaimoole R, Pecot CV, Dalton HJ, Hernandez A, Lokshin A, et al. Antagonism of tumoral prolactin receptor promotes autophagy-related cell death. Cell reports. 2014; 7:488-500.
18. Liu Y, Shoji-Kawata S, Sumpter RM, Jr., Wei Y, Ginet V, Zhang L, Posner B, Tran KA, Green DR, Xavier RJ, Shaw SY, Clarke PG, Puyal J and Levine B. Autosis is a Na+,K+-ATPase-regulated form of cell death triggered by autophagy-inducing peptides, starvation, and hypoxiaischemia. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110:20364-20371.
19. Wang Y, Li X, Wang L, Ding P, Zhang Y, Han W and Ma D. An alternative form of paraptosis-like cell death, triggered by TAJ/TROY and enhanced by PDCD5 overexpression. Journal of cell science. 2004; 117:1525-1532.
20. Overholtzer M, Mailleux AA, Mouneimne G, Normand G, Schnitt SJ, King RW, Cibas ES and Brugge JS. A nonapoptotic cell death process, entosis, that occurs by cellin-cell invasion. Cell. 2007; 131:966-979.
21. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, Morrison B, 3rd and Stockwell BR. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012; 149:1060-1072.
22. Edinger AL and Thompson CB. Death by design: apoptosis, necrosis and autophagy. Current opinion in cell biology. 2004; 16:663-669.
23. Kumar D, Shankar S and Srivastava RK. Rottlerin-induced autophagy leads to the apoptosis in breast cancer stem cells: molecular mechanisms. Molecular cancer. 2013; 12:171.
24. Kumar D, Shankar S and Srivastava RK. Rottlerin induces autophagy and apoptosis in prostate cancer stem cells via PI3K/Akt/mTOR signaling pathway. Cancer letters. 2014; 343:179-189.
25. Roca H, Varsos Z and Pienta KJ. CCL2 protects prostate cancer PC3 cells from autophagic death via phosphatidylinositol 3-kinase/AKT-dependent survivin upregulation. J Biol Chem. 2008; 283:25057-25073.
26. White E and DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clin Cancer Res. 2009; 15:5308-5316.
27. Codogno P, Mehrpour M and Proikas-Cezanne T. Canonical and non-canonical autophagy: variations on a common theme of self-eating? Nat Rev Mol Cell Bio. 2012; 13:7-12.
28. Kim JY, Zhao H, Martinez J, Doggett TA, Kolesnikov AV, Tang PH, Ablonczy Z, Chan CC, Zhou Z, Green DR and Ferguson TA. Noncanonical autophagy promotes the visual cycle. Cell. 2013; 154:365-376.
29. Keating AK, Kim GK, Jones AE, Donson AM, Ware K, Mulcahy JM, Salzberg DB, Foreman NK, Liang X, Thorburn A and Graham DK. Inhibition of Mer and Axl receptor tyrosine kinases in astrocytoma cells leads to increased apoptosis and improved chemosensitivity. Molecular cancer therapeutics. 2010; 9:1298-1307.
30. Liu Y, Liu JH, Chai K, Tashiro S, Onodera S and Ikejima T. Inhibition of c-Met promoted apoptosis, autophagy and loss of the mitochondrial transmembrane potential in oridonininduced A549 lung cancer cells. The Journal of pharmacy and pharmacology. 2013; 65:1622-1642.
31. Kong D, Heath E, Chen W, Cher M, Powell I, Heilbrun L, Li Y, Ali S, Sethi S, Hassan O, Hwang C, Gupta N, Chitale D, Sakr WA, Menon M and Sarkar FH. Epigenetic silencing of miR-34a in human prostate cancer cells and tumor tissue specimens can be reversed by BR-DIM treatment. American journal of translational research. 2012; 4:14-23.
32. Schaefer A, Jung M, Mollenkopf HJ, Wagner I, Stephan C, Jentzmik F, Miller K, Lein M, Kristiansen G and Jung K. Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma. International journal of cancer Journal international du cancer. 2010; 126:1166-1176.
33. Tong AW, Fulgham P, Jay C, Chen P, Khalil I, Liu S, Senzer N, Eklund AC, Han J and Nemunaitis J. MicroRNA profile analysis of human prostate cancers. Cancer gene therapy. 2009; 16:206-216.
34. Corcoran C, Rani S and O'Driscoll L. miR-34a is an intracellular and exosomal predictive biomarker for response to docetaxel with clinical relevance to prostate cancer progression. The Prostate. 2014; 74:1320-1334.
35. Guzel E, Karatas OF, Semercioz A, Ekici S, Aykan S, Yentur S, Creighton CJ, Ittmann M and Ozen M. Identification of microRNAs differentially expressed in prostatic secretions of patients with prostate cancer. International journal of cancer Journal international du cancer. 2015; 136:875-9.
36. Bowman K and Leong KW. Chitosan nanoparticles for oral drug and gene delivery. International journal of nanomedicine. 2006; 1:117-128.
37. Han HD, Mangala LS, Lee JW, Shahzad MM, Kim HS, Shen D, Nam EJ, Mora EM, Stone RL, Lu C, Lee SJ, Roh JW, Nick AM, Lopez-Berestein G and Sood AK. Targeted gene silencing using RGD-labeled chitosan nanoparticles. Clin Cancer Res. 2010; 16:3910-3922.
38. Kang R, Zeh HJ, Lotze MT and Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell death and differentiation. 2011; 18:571-580.
39. Kihara A, Kabeya Y, Ohsumi Y and Yoshimori T. Beclinphosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO reports. 2001; 2:330-335.
40. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012; 8:445-544.
41. Kimura S, Noda T and Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007; 3:452-460.
42. Puissant A, Fenouille N and Auberger P. When autophagy meets cancer through p62/SQSTM1. Am J Cancer Res. 2012; 2:397-413.
43. Amaravadi RK, Lippincott-Schwartz J, Yin XM, Weiss WA, Takebe N, Timmer W, DiPaola RS, Lotze MT and White E. Principles and current strategies for targeting autophagy for cancer treatment. Clinical cancer research: an official journal of the American Association for Cancer Research. 2011; 17:654-666.
44. Chang TK, Shravage BV, Hayes SD, Powers CM, Simin RT, Wade Harper J and Baehrecke EH. Uba1 functions in Atg7-and Atg3-independent autophagy. Nature cell biology. 2013; 15:1067-1078.
45. Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, Komatsu M, Otsu K, Tsujimoto Y and Shimizu S. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature. 2009; 461:654-658.
46. Cecconi F and Levine B. The role of autophagy in mammalian development: cell makeover rather than cell death. Developmental cell. 2008; 15:344-357.
47. Shi Y, Han JJ, Tennakoon JB, Mehta FF, Merchant FA, Burns AR, Howe MK, McDonnell DP and Frigo DE. Androgens promote prostate cancer cell growth through induction of autophagy. Molecular endocrinology. 2013; 27:280-295.
48. Chen Y, Liu XR, Yin YQ, Lee CJ, Wang FT, Liu HQ, Wu XT and Liu J. Unravelling the multifaceted roles of Atg proteins to improve cancer therapy. Cell proliferation. 2014; 47:105-112.
49. Nakatogawa H, Ishii J, Asai E and Ohsumi Y. Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy. 2012; 8:177-186.
50. Rothe K, Lin H, Lin KB, Leung A, Wang HM, Malekesmaeili M, Brinkman RR, Forrest DL, Gorski SM and Jiang X. The core autophagy protein ATG4B is a potential biomarker and therapeutic target in CML stem/progenitor cells. Blood. 2014; 123:3622-3634.
51. Araujo JC, Trudel GC, Saad F, Armstrong AJ, Yu EY, Bellmunt J, Wilding G, McCaffrey J, Serrano SV, Matveev VB, Efstathiou E, Oudard S, Morris MJ, Sizer B, Goebell PJ, Heidenreich A, et al. Docetaxel and dasatinib or placebo in men with metastatic castration-resistant prostate cancer (READY): a randomised, double-blind phase 3 trial. The Lancet Oncology. 2013; 14:1307-1316.
52. Keller ET and Brown J. Prostate cancer bone metastases promote both osteolytic and osteoblastic activity. Journal of cellular biochemistry. 2004; 91:718-729.
53. Sturge J, Caley MP and Waxman J. Bone metastasis in prostate cancer: emerging therapeutic strategies. Nature reviews Clinical oncology. 2011; 8:357-368.
54. Clark PM, Loher P, Quann K, Brody J, Londin ER and Rigoutsos I. Argonaute CLIP-Seq reveals miRNA targetome diversity across tissue types. Scientific reports. 2014; 4:5947.
55. Scarlatti F, Maffei R, Beau I, Codogno P and Ghidoni R. Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell death and differentiation. 2008; 15:1318-1329.
56. Liu K, Huang J, Xie M, Yu Y, Zhu S, Kang R, Cao L, Tang D and Duan X. MIR34A regulates autophagy and apoptosis by targeting HMGB1 in the retinoblastoma cell. Autophagy. 2014; 10:442-452.
57. Lu C, Han HD, Mangala LS, Ali-Fehmi R, Newton CS, Ozbun L, Armaiz-Pena GN, Hu W, Stone RL, Munkarah A, Ravoori MK, Shahzad MM, Lee JW, Mora E, Langley RR, Carroll AR, et al. Regulation of tumor angiogenesis by EZH2. Cancer cell. 2010; 18:185-197.