Macrophages mediate gemcitabine resistance of pancreatic adenocarcinoma by upregulating cytidine deaminase

Oncogene

Volumn 33, Issue 29, 2014, Pages 3812-3819

  Weizman, N ^a   Krelin, Y ^a   Shabtay Orbach, A ^a   Amit, M ^a   Binenbaum, Y ^a   Wong, R J ^b   Gil, Z ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

chemotherapy; gemcitabine; macrophages; cytidine deaminase; pancreatic ductal adenocarcinoma; resistance

Indexed keywords

CASPASE 3; CYTIDINE DEAMINASE; GEMCITABINE; GW 2580; PHOSPHOTRANSFERASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CANCER CELL; CANCER RESISTANCE; CELL MIGRATION; CELL TRANSPORT; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME METABOLISM; FEMALE; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

MUS; MUS MUSCULUS;

ADENOCARCINOMA; ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; CELL LINE, TUMOR; CYTIDINE DEAMINASE; DEOXYCYTIDINE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MACROPHAGES; MICE; MICE, KNOCKOUT; PANCREATIC NEOPLASMS; RECEPTORS, GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84904661611     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.357     Document Type: Article

References (49)

1. Colucci G, Labianca R, Di Costanzo F, Gebbia V, Carteni G, Massidda B et al. Randomized phase III trial of gemcitabine plus cisplatin compared with singleagent gemcitabine as first-line treatment of patients with advanced pancreatic cancer: the GIP-1 study. J Clin Oncol 2010; 28: 1645-1651
2. Cunningham D, Chau I, Stocken DD, Valle JW, Smith D, Steward W et al. Phase III randomized comparison of gemcitabine versus gemcitabine plus capecitabine in patients with advanced pancreatic cancer. J Clin Oncol 2009; 27: 5513-5518
3. Tempero M, Plunkett W, Ruiz Van Haperen V, Hainsworth J, Hochster H, Lenzi R et al. Randomized phase II comparison of dose-intense gemcitabine: thirty-minute infusion and fixed dose rate infusion in patients with pancreatic adenocarcinoma. J Clin Oncol 2003; 21: 3402-3408
4. Loehrer Sr PJ, Feng Y, Cardenes H, Wagner L, Brell JM, Cella D et al. Gemcitabine alone versus gemcitabine plus radiotherapy in patients with locally advanced pancreatic cancer: an Eastern Cooperative Oncology Group trial. J Clin Oncol 2011; 29: 4105-4112
5. Giovannetti E, Mey V, Nannizzi S, Pasqualetti G, Del Tacca M, Danesi R. Pharmacogenetics of anticancer drug sensitivity in pancreatic cancer. Mol Cancer Therap 2006; 5: 1387-1395
6. Summy JM, Trevino JG, Baker CH, Gallick GE. c-Src regulates constitutive and EGFmediated VEGF expression in pancreatic tumor cells through activation of phosphatidyl inositol-3 kinase and p38 MAPK. Pancreas 2005; 31: 263-274
7. Greten FR, Weber CK, Greten TF, Schneider G, Wagner M, Adler G et al. Stat3 and NF-kappaB activation prevents apoptosis in pancreatic carcinogenesis. Gastroenterology 2002; 123: 2052-2063
8. Korc M. Pancreatic cancer-Associated stroma production. Am J Surg 2007; 194 (Suppl 4): S84-S86
9. Andre F, Berrada N, Desmedt C. Implication of tumor microenvironment in the resistance to chemotherapy in breast cancer patients. Curr Opin Oncol 2010; 22: 547-551
10. Ricci F, Kern SE, Hruban RH, Iacobuzio-Donahue CA. Stromal responses to carcinomas of the pancreas: juxtatumoral gene expression conforms to the infiltrating pattern and not the biologic subtype. Cancer Biol Ther 2005; 4: 302-307
11. Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 2010; 22: 231-237
12. Esposito I, Menicagli M, Funel N, Bergmann F, Boggi U, Mosca F et al. Inflammatory cells contribute to the generation of an angiogenic phenotype in pancreatic ductal adenocarcinoma. J Clin Pathol 2004; 57: 630-636
13. Jinushi M, Chiba S, Yoshiyama H, Masutomi K, Kinoshita I, Dosaka-Akita H et al. Tumor-Associated macrophages regulate tumorigenicity and anticancer drug responses of cancer stem/initiating cells. Proc Natl Acad Sci USA 2011; 108: 12425-12430
14. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009; 9: 239-252
15. Gil Z, Cavel O, Kelly K, Brader P, Rein A, Gao SP et al. Paracrine regulation of pancreatic cancer cell invasion by peripheral nerves. J Natl Cancer Inst 2010; 102: 107-118
16. Cavel O, Shomron O, Shabtay A, Vital J, Trejo-Leider L, Weizman N et al. Endoneurial macrophages induce perineural invasion of pancreatic cancer cells by secretion of GDNF and activation of RET tyrosine kinase receptor. Cancer Res 2012; 72: 5733-5743
17. Nefedova Y, Landowski TH, Dalton WS. Bone marrow stromal-derived soluble factors and direct cell contact contribute to de novo drug resistance of myeloma cells by distinct mechanisms. Leukemia 2003; 17: 1175-1182
18. Zheng Y, Cai Z, Wang S, Zhang X, Qian J, Hong S et al. Macrophages are an abundant component of myeloma microenvironment and protect myeloma cells from chemotherapy drug-induced apoptosis. Blood 2009; 114: 3625-3628
19. Staroselsky AN, Fan D, OBrian CA, Bucana CD, Gupta KP, Fidler IJ. Site-dependent differences in response of the UV-2237 murine fibrosarcoma to systemic therapy with adriamycin. Cancer Res 1990; 50: 7775-7780
20. Meads MB, Hazlehurst LA, Dalton WS. The bone marrow microenvironment as a tumor sanctuary and contributor to drug resistance. Clin Cancer Res 2008; 14: 2519-2526
21. Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006; 124: 263-266
22. De Palma M, Lewis CE. Cancer: Macrophages limit chemotherapy. Nature 2011; 472: 303-304
23. Mitchem JB, Brennan DJ, Knolhoff BL, Belt BA, Zhu Y, Sanford DE et al. Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res 2013; 73: 1128-1141
24. Ferrandina G, Ludovisi M, Lorusso D, Pignata S, Breda E, Savarese A et al. Phase III trial of gemcitabine compared with pegylated liposomal doxorubicin in progressive or recurrent ovarian cancer. J Clin Oncol 2008; 26: 890-896
25. Morgan MA, Parsels LA, Parsels JD, Mesiwala AK, Maybaum J, Lawrence TS. Role of checkpoint kinase 1 in preventing premature mitosis in response to gemcitabine. Cancer Res 2005; 65: 6835-6842
26. Schafer H, Struck B, Feldmann EM, Bergmann F, Grage-Griebenow E, Geismann C et al. TGF-beta1-dependent L1CAM expression has an essential role in macrophage-induced apoptosis resistance and cell migration of human intestinal epithelial cells. Oncogene 2013; 32: 180-189
27. Clark CE, Hingorani SR, Mick R, Combs C, Tuveson DA, Vonderheide RH. Dynamics of the immune reaction to pancreatic cancer from inception to invasion. Cancer Res 2007; 67: 9518-9527
28. Zhang J, Lu Y, Pienta KJ. Multiple roles of chemokine (C-C motif) ligand 2 in promoting prostate cancer growth. J Natl Cancer Inst 2010; 102: 522-528
29. Pahler JC, Tazzyman S, Erez N, Chen YY, Murdoch C, Nozawa H et al. Plasticity in tumor-promoting inflammation: impairment of macrophage recruitment evokes a compensatory neutrophil response. Neoplasia 2008; 10: 329-340
30. Niedergethmann M, Alves F, Neff JK, Heidrich B, Aramin N, Li L et al. Gene expression profiling of liver metastases and tumour invasion in pancreatic cancer using an orthotopic SCID mouse model. Br J Cancer 2007; 97: 1432-1440
31. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009; 324: 1457-1461
32. van Rooijen N, van Kesteren-Hendrikx E. In vivo depletion of macrophages by liposome-mediated suicide. Methods Enzymol 2003; 373: 3-16
33. Steube KG, Meyer C, Drexler HG. Secretion of functional hematopoietic growth factors by human carcinoma cell lines. Int J Cancer 1998; 78: 120-124
34. Green CE, Liu T, Montel V, Hsiao G, Lester RD, Subramaniam S et al. Chemoattractant signaling between tumor cells and macrophages regulates cancer cell migration, metastasis and neovascularization. PLoS ONE 2009; 4: e6713
35. Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, Hruban RH et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005; 7: 469-483
36. Bhutia YD, Hung SW, Patel B, Lovin D, Govindarajan R. CNT1 expression influences proliferation and chemosensitivity in drug-resistant pancreatic cancer cells. Cancer Res 2011; 71: 1825-1835
37. Akita H, Zheng Z, Takeda Y, Kim C, Kittaka N, Kobayashi S et al. Significance of RRM1 and ERCC1 expression in resectable pancreatic adenocarcinoma. Oncogene 2009; 28: 2903-2909
38. Burris 3rd HA, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol 1997; 15: 2403-2413
39. Gilbert LA, Hemann MT. Chemotherapeutic resistance: surviving stressful situations. Cancer Res 2011; 71: 5062-5066
40. Straussman R, Morikawa T, Shee K, Barzily-Rokni M, Qian ZR, Du J et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012; 487: 500-504
41. Yamashina K, Miller BE, Heppner GH. Macrophage-mediated induction of drugresistant variants in a mouse mammary tumor cell line. Cancer Res 1986; 46: 2396-2401
42. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer discovery 2011; 1: 54-67
43. Shree T, Olson OC, Elie BT, Kester JC, Garfall AL, Simpson K et al. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev 2011; 25: 2465-2479
44. Ahn GO, Tseng D, Liao CH, Dorie MJ, Czechowicz A, Brown JM. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc Natl Acad Sci USA 2010; 107: 8363-8368
45. Kozin SV, Kamoun WS, Huang Y, Dawson MR, Jain RK, Duda DG. Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation. Cancer Res 2010; 70: 5679-5685
46. Vakkila J, Lotze MT. Inflammation and necrosis promote tumour growth. Nat Rev Immunol 2004; 4: 641-648
47. Dijkgraaf EM, Heusinkveld M, Tummers B, Vogelpoel LT, Goedemans R, Jha V et al. Chemotherapy alters monocyte differentiation to favor generation of cancersupporting M2 macrophages in the tumor microenvironment. Cancer Res 2013; 73: 2480-2492
48. Singh S, Srivastava SK, Bhardwaj A, Owen LB, Singh AP. CXCL12-CXCR4 signalling axis confers gemcitabine resistance to pancreatic cancer cells: a novel target for therapy. Br J Cancer 2010; 103: 1671-1679
49. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012; 487: 505-509.