Bisphosphonates inhibit stellate cell activity and enhance antitumor effects of nanoparticle albumin-bound paclitaxel in pancreatic ductal adenocarcinoma

Molecular Cancer Therapeutics

Volumn 13, Issue 11, 2014, Pages 2583-2594

  Gonzalez Villasana, Vianey ^a   Rodriguez Aguayo, Cristian ^a   Arumugam, Thiruvengadam ^a   Cruz Monserrate, Zobeida ^a   Fuentes Mattei, Enrique ^a   Deng, Defeng ^a   Hwang, Rosa F ^a   Wang, Huamin ^a   Ivan, Cristina ^a   Garza, Raul Joshua ^a   Cohen, Evan ^a   Gao, Hui ^a   Armaiz Pena, Guillermo N ^a   Monroig Bosque, Paloma Del C ^a,b   Philip, Bincy ^a   Rashed, Mohammed H ^a,c   Aslan, Burcu ^a   Erdogan, Mumin Alper ^a   Gutierrez Puente, Yolanda ^d   Ozpolat, Bulent ^a   Reuben, James M ^a   Sood, Anil K ^a   Logsdon, Craig ^a   Lopez Berestein, Gabriel ^a   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

^c AL AZHAR UNIVERSITY   (Egypt)

^d UNIVERSIDAD AUTÓNOMA DE NUEVO LEÓN   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA NAPHTHYL BUTYRATE ESTERASE; ALPHA SMOOTH MUSCLE ACTIN; CASPASE 3; CAVEOLIN 1; COLLAGEN TYPE 1; ESTERASE; GEMCITABINE; MEVALONIC ACID; MONOCYTE CHEMOTACTIC PROTEIN 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PACLITAXEL; PAMIDRONIC ACID; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; UNCLASSIFIED DRUG; ZOLEDRONIC ACID; ALBUMINOID; BISPHOSPHONIC ACID DERIVATIVE; NANOPARTICLE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BONE MARROW; CANCER TRANSPLANTATION; CELL ACTIVATION; CELL ACTIVITY; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINEAGE; CELL PROLIFERATION; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; CYSTIC FIBROSIS; DOSE RESPONSE; DRUG EFFECT; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MONOCYTE; MOUSE; NICK END LABELING; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREATIC STELLATE CELL; PRENYLATION; PROTEIN EXPRESSION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR VOLUME; WESTERN BLOTTING; ADULT; ANIMAL; CARCINOMA, PANCREATIC DUCTAL; DRUG EFFECTS; DRUG POTENTIATION; DRUG SCREENING; IMMUNOHISTOCHEMISTRY; NUDE MOUSE; PANCREATIC NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

ADULT; ALBUMINS; ANIMALS; APOPTOSIS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CELL PROLIFERATION; DIPHOSPHONATES; DRUG SYNERGISM; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, NUDE; NANOPARTICLES; PACLITAXEL; PANCREATIC NEOPLASMS; PANCREATIC STELLATE CELLS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84918774527     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-14-0028     Document Type: Article

References (50)

1. Omary MB, Lugea A, Lowe AW, Pandol SJ. The pancreatic stellate cell: a star on the rise in pancreatic diseases. J Clin Invest 2007;117:50-9.
2. Tassone P, Tagliaferri P, Viscomi C, Palmieri C, Caraglia M, D'Alessandro A, et al. Zoledronic acid induces antiproliferative and apoptotic effects in human pancreatic cancer cells in vitro. Br J Cancer 2003;88:1971-8.
3. Korc M. Pancreatic cancer-associated stroma production. Am J Surg 2007;194:S84-6.
4. Erkan M, Hausmann S, Michalski CW, Fingerle AA, Dobritz M, Kleeff J, et al. The role of stroma in pancreatic cancer: diagnostic and therapeutic implications. Nat Rev Gastroenterol Hepatol 2012;9:454-67.
5. Phillips P. Pancreatic stellate cells and fibrosis. In: Grippo PJ, Munshi HG, editors. Pancreatic cancer and tumor microenvironment. Trivandrum, India: Transworld Research Network; 2012. Chapter 3.
6. Vonlaufen A, Joshi S, Qu C, Phillips PA, Xu Z, Parker NR, et al. Pancreatic stellate cells: partners in crimewith pancreatic cancer cells. Cancer Res 2008;68:2085-93.
7. Masamune A, Shimosegawa T. Signal transduction in pancreatic stellate cells. J Gastroenterol 2009;44:249-60.
8. Apte MV, Wilson JS. Dangerous liaisons: pancreatic stellate cells and pancreatic cancer cells. J Gastroenterol Hepatol 2012;27:69-74.
9. Shimizu K, Kobayashi M, Tahara J, Shiratori K. Cytokines and peroxisome proliferator-activated receptor gamma ligand regulate phagocytosis by pancreatic stellate cells. Gastroenterology 2005;128:2105-18.
10. Masamune A, Kikuta K, Watanabe T, Satoh K, Satoh A, Shimosegawa T. Pancreatic stellate cells express Toll-like receptors. J Gastroenterol 2008;43:352-62.
11. Rogers MJ, Chilton KM, Coxon FP, Lawry J, Smith MO, Suri S, et al. Bisphosphonates induce apoptosis in mouse macrophage-like cells in vitro by a nitric oxide-independent mechanism. J Bone Miner Res 1996;11:1482-91.
12. Rogers TL, Holen I. Tumour macrophages as potential targets of bisphosphonates. J Transl Med 2011;9:1-17.
13. Thompson K, Rogers MJ, Coxon FP, Crockett JC. Cytosolic entry of bisphosphonate drugs requires acidi fi cation of vesicles after fluid-phase endocytosis. Mol Pharmacol 2006;69:1624-32.
14. Green J, Clezardin P. The molecular basis of bisphosphonate activity: a preclinical perspective. Semin Oncol 2010;37(Suppl 1):S3-11.
15. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, et al. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 2008;68:918-26.
16. Freireich EJ, Gehan EA, Rall DP, Schmidt LH, Skipper HE. Quantitative comparison of toxicity of anticancer agents in mouse, rat, hamster, dog, monkey, and man. Cancer Chemother Rep 1966;50:219-44.
17. Administration FaD. Guidance for industry estimating the maximum safe starting dose in initial clinical trials for therapeutics in adult healthy volunteers. [July 6, 2005]. Available from: http://www.fda.gov/downloads/Drugs/Guidances/UCM078932.pdf.
18. Bergner R, Diel IJ, Henrich D, Hoffmann M, Uppenkamp M. Differences in nephrotoxicity of intravenous bisphosphonates for the treatment of malignancy-related bone disease. Onkologie 2006;29:534-40.
19. Vivas-Mejia PE, Rodriguez-Aguayo C, Han HD, Shahzad MM, Valiyeva F, Shibayama M, et al. Silencing survivin splice variant 2B leads to antitumor activity in taxane-resistant ovarian cancer. Clin Cancer Res 2011;17:3716-26.
20. Stone RM, Imamura K, Datta R, Sherman ML, Kufe DW. Inhibition of phorbol ester-induced monocytic differentiation and c-fms gene expression by dexamethasone: potential involvement of arachidonic acid metabolites. Blood 1990;76:1225-32.
21. Barendsen N, Mueller M, Chen B. Inhibition of TPA-induced monocytic differentiation in THP-1 human monocytic leukemic cells by staurosporine, a potent protein kinase C inhibitor. Leuk Res 1990;14:467-74.
22. Reynolds NJ, Baldassare JJ, Henderson PA, Shuler JL, Ballas LM, Burns DJ, et al. Translocation and downregulation of protein kinase C isoenzymes-alpha and -epsilon by phorbol ester and bryostatin-1 in human keratinocytes and fibroblasts. J Invest Dermatol 1994;103:364-9.
23. Mehta K, Claringbold P, Lopez-Berestein G. Suppression of macrophage cytostatic activation by serum retinoids: a possible role for transglutaminase. J Immunol 1987;138:3902-6.
24. Mehta K, Lopez-Berestein G. Expression of tissue transglutaminase in cultured monocytic leukemia (THP-1) cells during differentiation. Cancer Res 1986;46:1388-94.
25. Michailidou M, Brown HK, Le fley DV, Evans A, Cross SS, Coleman RE, et al. Microvascular endothelial cell responses in vitro and in vivo: modulation by zoledronic acid and paclitaxel? J Vasc Res 2010;47:481-93.
26. Holen I, Coleman RE. Anti-tumour activity of bisphosphonates in preclinical models of breast cancer. Breast Cancer Res 2010;12:214.
27. Wakchoure S, Merrell MA, Aldrich W, Millender-Swain T, Harris KW, Triozzi P, et al. Bisphosphonates inhibit the growth of mesothelioma cells in vitro and in vivo. Clin Cancer Res 2006;12:2862-8.
28. Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 2009;29:313-26.
29. Bachem MG, Zhou Z, Zhou S, Siech M. Role of stellate cells in pancreatic fibrogenesis associated with acute and chronic pancreatitis. J Gastroenterol Hepatol 2006;21(Suppl 3):S92-6.
30. Masamune A, Kikuta K, Watanabe T, Satoh K, Hirota M, Hamada S, et al. Fibrinogen induces cytokine and collagen production in pancreatic stellate cells. Gut 2009;58:550-9.
31. Bailey JM, Swanson BJ, Hamada T, Eggers JP, Singh PK, Caffery T, et al. Sonic hedgehog promotes desmoplasia in pancreatic cancer. Clin Cancer Res 2008;14:5995-6004.
32. Hlavaty J, Petznek H, Holzmuller H, Url A, Jandl G, Berger A, et al. Evaluation of a gene-directed enzyme-product therapy (GDEPT) in human pancreatic tumor cells and their use as in vivo models for pancreatic cancer. PLoS ONE 2012;7:e40611.
33. Rosen LS, Gordon D, Kaminski M, Howell A, Belch A, Mackey J, et al. Long-term efficacy and safety of zoledronic acid compared with pamidronate disodium in the treatment of skeletal complications in patients with advanced multiple myeloma or breast carcinoma: a randomized, double-blind, multicenter, comparative trial. Cancer 2003;98:1735-44.
34. Miele E, Spinelli GP, Miele E, Tomao F, Tomao S. Albumin-bound formulation of paclitaxel (Abraxane ABI-007) in the treatment of breast cancer. Int J Nanomed 2009;4:99-105.
35. Desai N, Trieu V, Yao Z, Louie L, Ci S, Yang A, et al. Increased antitumor activity, intratumor paclitaxel concentrations, and endothelial cell transport of cremophor-free, albumin-bound paclitaxel, ABI-007, compared with cremophor-based paclitaxel. Clin Cancer Res 2006;12:1317-24.
36. Lippi U, Cappelletti P, Schinella M. Alpha-naphthyl butyrate esterase (a selective cytochemical monocyte marker). Ric Clin Lab 1983;13:467-71.
37. Takiguchi S, Nishino Y, Inoue K, Ikeda M, Kataoka Y, Matsusue K, et al. The bisphosphonate incadronate inhibits intraperitoneal dissemination in an in vivo pancreatic cancer model. Oncol Rep 2012;28:111-6.
38. Hashimoto K, Morishige K, Sawada K, Tahara M, Kawagishi R, Ikebuchi Y, et al. Alendronate inhibits intraperitoneal dissemination in in vivo ovarian cancer model. Cancer Res 2005;65:540-5.
39. Vonlaufen A, Phillips PA, Xu Z, Goldstein D, Pirola RC, Wilson JS, et al. Pancreatic stellate cells and pancreatic cancer cells: an unholy alliance. Cancer Res 2008;68:7707-10.
40. Lohr M, Trautmann B, Gottler M, Peters S, Zauner I, Maillet B, et al. Human ductal adenocarcinomas of the pancreas express extracellular matrix proteins. Br J Cancer 1994;69:144-51.
41. Bachem MG, Schunemann M, Ramadani M, Siech M, Beger H, Buck A, et al. Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. Gastroenterology 2005;128:907-21.
42. Gharaee-Kermani M, Denholm EM, Phan SH. Costimulation of fibroblast collagen and transforming growth factor beta1 gene expression by monocyte chemoattractant protein-1 via specific receptors. J Biol Chem 1996;271:17779-84.
43. Monti P, Leone BE, Marchesi F, Balzano G, Zerbi A, Scaltrini F, et al. The CC chemokine MCP-1/CCL2 in pancreatic cancer progression: regulation of expression and potential mechanisms of antimalignant activity. Cancer Res 2003;63:7451-61.
44. Chehl N, Gong Q, Chipitsyna G, Aziz T, Yeo CJ, Arafat HA. Angiotensin II regulates the expression of monocyte chemoattractant protein-1 in pancreatic cancer cells. J Gastrointest Surg 2009;13:2189-200.
45. Graves DT, Barnhill R, Galanopoulos T, Antoniades HN. Expression of monocyte chemotactic protein-1 in human melanoma in vivo. Am J Pathol 1992;140:9-14.
46. Negus RP, Stamp GW, Relf MG, Burke F, Malik ST, Bernasconi S, et al. The detection and localization of monocyte chemoattractant protein-1 (MCP-1) in human ovarian cancer. J Clin Invest 1995;95:2391-6.
47. Koide N, Nishio A, Sato T, Sugiyama A, Miyagawa S. Significance of macrophage chemoattractant protein-1 expression and macrophage infiltration in squamous cell carcinoma of the esophagus. Am J Gastroenterol 2004;99:1667-74.
48. Wynn TA, Barron L. Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis 2010;30:245-57.
49. Zhao M, Tominaga Y, Ohuchida K, Mizumoto K, Cui L, Kozono S, et al. Significance of combination therapy of zoledronic acid and gemcitabine on pancreatic cancer. Cancer Sci 2012;103:58-66.
50. Shi Z, Azuma A, Sampath D, Li YX, Huang P, Plunkett W. S-Phase arrest by nucleoside analogues and abrogation of survival without cell cycle progression by 7-hydroxystaurosporine. Cancer Res 2001;61:1065-72.