Mesenchymal Stem Cells Promote Pancreatic Tumor Growth by Inducing Alternative Polarization of Macrophages

Neoplasia (United States)

Volumn 18, Issue 3, 2016, Pages 142-151

  Mathew, Esha ^a   Brannon, Arthur L ^a   Del Vecchio, AnnaChiara ^a   Garcia, Paloma E ^a   Penny, Morgan K ^a   Kane, Kevin T ^a   Vinta, Alekya ^a   Buckanovich, Ronald J ^a,b   di Magliano, Marina Pasca ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL POLARITY; CONTROLLED STUDY; FIBROBLAST; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MESENCHYMAL STEM CELL; MONOCYTE; MOUSE; NONHUMAN; PANCREAS CANCER; PANCREATIC STELLATE CELL; PRIORITY JOURNAL; STROMA CELL; TUMOR GROWTH; CELL PROLIFERATION; GENETICS; HUMAN; MESENCHYMAL STROMA CELL; PANCREAS; PANCREAS TUMOR; PATHOLOGY; TUMOR MICROENVIRONMENT;

CELL DIFFERENTIATION; CELL POLARITY; CELL PROLIFERATION; HUMANS; MACROPHAGES; MESENCHYMAL STROMAL CELLS; PANCREAS; PANCREATIC NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84963978902     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2016.01.005     Document Type: Article

References (36)

1. Neesse A, Michl P, Frese KK, Feig C, Cook N, Jacobetz MA, Lolkema MP, Buchholz M, Olive KP, Gress TM, et al. Stromal biology and therapy in pancreatic cancer. Gut 2011, 60:861-868.
2. Hruban RH, Maitra A, Goggins M Update on pancreatic intraepithelial neoplasia. Int J Clin Exp Pathol 2008, 1:306-316.
3. 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.
4. Apte MV, Park S, Phillips PA, Santucci N, Goldstein D, Kumar RK, Ramm GA, Buchler M, Friess H, McCarroll JA, et al. Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas 2004, 29:179-187.
5. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, Ji B, Evans DB, Logsdon CD Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 2008, 68:918-926.
6. Ozdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, Laklai H, Sugimoto H, Kahlert C, Novitskiy SV, et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 2014, 25:719-734.
7. Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, Dekleva EN, Saunders T, Becerra CP, Tattersall IW, et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 2014, 25:735-747.
8. Baertschiger RM, Bosco D, Morel P, Serre-Beinier V, Berney T, Buhler LH, Gonelle-Gispert C Mesenchymal stem cells derived from human exocrine pancreas express transcription factors implicated in beta-cell development. Pancreas 2008, 37:75-84.
9. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3:301-313.
10. Joyce JA, Pollard JW Microenvironmental regulation of metastasis. Nat Rev Cancer 2009, 9:239-252.
11. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007, 449:557-563.
12. McLean K, Gong Y, Choi Y, Deng N, Yang K, Bai S, Cabrera L, Keller E, McCauley L, Cho KR, et al. Human ovarian carcinoma-associated mesenchymal stem cells regulate cancer stem cells and tumorigenesis via altered BMP production. J Clin Invest 2011, 121:3206-3219.
13. Ren G, Zhao X, Wang Y, Zhang X, Chen X, Xu C, Yuan ZR, Roberts AI, Zhang L, Zheng B, et al. CCR2-dependent recruitment of macrophages by tumor-educated mesenchymal stromal cells promotes tumor development and is mimicked by TNFalpha. Cell Stem Cell 2012, 11:812-824.
14. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, Ross S, Conrads TP, Veenstra TD, Hitt BA, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003, 4:437-450.
15. Biankin AV, Waddell N, Kassahn KS, Gingras MC, Muthuswamy LB, Johns AL, Miller DK, Wilson PJ, Patch AM, Wu J, et al. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 2012, 491:399-405.
16. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321:1801-1806.
17. Gopurappilly R, Bhat V, Bhonde R Pancreatic tissue resident mesenchymal stromal cell (MSC)-like cells as a source of in vitro islet neogenesis. J Cell Biochem 2013, 114:2240-2247.
18. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
19. Mathew E, Collins MA, Fernandez-Barrena MG, Holtz AM, Yan W, Hogan JO, Tata Z, Allen BL, Fernandez-Zapico ME, di Magliano MP The transcription factor GLI1 modulates the inflammatory response during pancreatic tissue remodeling. J Biol Chem 2014, 289:27727-27743.
20. Lesina M, Kurkowski MU, Ludes K, Rose-John S, Treiber M, Kloppel G, Yoshimura A, Reindl W, Sipos B, Akira S, et al. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell 2011, 19:456-469.
21. Zhang Y, Yan W, Collins MA, Bednar F, Rakshit S, Zetter BR, Stanger BZ, Chung I, Rhim AD, di Magliano MP Interleukin-6 is required for pancreatic cancer progression by promoting MAPK signaling activation and oxidative stress resistance. Cancer Res 2013, 73:6359-6374.
22. Sharma S, Stolina M, Lin Y, Gardner B, Miller PW, Kronenberg M, Dubinett SM T cell-derived IL-10 promotes lung cancer growth by suppressing both T cell and APC function. J Immunol 1999, 163:5020-5028.
23. Amatangelo MD, Goodyear S, Varma D, Stearns ME c-Myc expression and MEK1-induced Erk2 nuclear localization are required for TGF-beta induced epithelial-mesenchymal transition and invasion in prostate cancer. Carcinogenesis 2012, 33:1965-1975.
24. Yeh TS, Wu CW, Hsu KW, Liao WJ, Yang MC, Li AF, Wang AM, Kuo ML, Chi CW The activated Notch1 signal pathway is associated with gastric cancer progression through cyclooxygenase-2. Cancer Res 2009, 69:5039-5048.
25. Collins MA, Brisset JC, Zhang Y, Bednar F, Pierre J, Heist KA, Galban CJ, Galban S, di Magliano MP Metastatic pancreatic cancer is dependent on oncogenic Kras in mice. PLoS One 2012, 7:e49707.
26. Jiang W, Zhang Y, Kane KT, Collins MA, Simeone DM, di Magliano MP, Nguyen KT CD44 regulates pancreatic cancer invasion through MT1-MMP. Mol Cancer Res 2015, 13:9-15.
27. Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, Hruban RH, Rustgi AK, Chang S, Tuveson DA Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005, 7:469-483.
28. Quante M, Tu SP, Tomita H, Gonda T, Wang SS, Takashi S, Baik GH, Shibata W, Diprete B, Betz KS, et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011, 19:257-272.
29. Kramann R, Schneider RK, DiRocco DP, Machado F, Fleig S, Bondzie PA, Henderson JM, Ebert BL, Humphreys BD Perivascular Gli1+ progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell 2015, 16:51-66.
30. Zhu Y, Knolhoff BL, Meyer MA, Nywening TM, West BL, Luo J, Wang-Gillam A, Goedegebuure SP, Linehan DC, DeNardo DG CSF1/CSF1R blockade reprograms tumor-infiltrating macrophages and improves response to T-cell checkpoint immunotherapy in pancreatic cancer models. Cancer Res 2014, 74:5057-5069.
31. Duffield JS, Forbes SJ, Constandinou CM, Clay S, Partolina M, Vuthoori S, Wu S, Lang R, Iredale JP Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest 2005, 115:56-65.
32. Feig C, Jones JO, Kraman M, Wells RJ, Deonarine A, Chan DS, Connell CM, Roberts EW, Zhao Q, Caballero OL, et al. Targeting CXCL12 from FAP-expressing carcinoma-associated fibroblasts synergizes with anti-PD-L1 immunotherapy in pancreatic cancer. Proc Natl Acad Sci U S A 2013, 110:20212-20217.
33. Erez N, Truitt M, Olson P, Arron ST, Hanahan D Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 2010, 17:135-147.
34. Weischenfeldt J, Porse B Bone marrow-derived macrophages (BMM): isolation and applications. CSH Protoc 2008, pdb prot5080 2008.
35. Cho DI, Kim MR, Jeong HY, Jeong HC, Jeong MH, Yoon SH, Kim YS, Ahn Y Mesenchymal stem cells reciprocally regulate the M1/M2 balance in mouse bone marrow-derived macrophages. Exp Mol Med 2014, 46:e70.
36. Zhang QZ, Su WR, Shi SH, Wilder-Smith P, Xiang AP, Wong A, Nguyen AL, Kwon CW, Le AD Human gingiva-derived mesenchymal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing. Stem Cells 2010, 28:1856-1868.