Characterization of adipose-derived stem cells from subcutaneous and visceral adipose tissues and their function in breast cancer cells

Oncotarget

Volumn 6, Issue 33, 2015, Pages 34475-34493

  Ritter, Andreas ^a   Friemel, Alexandra ^a   Fornoff, Friderike ^a   Adjan, Mouhib ^a   Solbach, Christine ^a   Yuan, Juping ^a   Louwen, Frank ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Adipose derived stem cells; Breast cancer cells; Drug resistance; Epithelial to mesenchymal transition; Invasion

Indexed keywords

BI 2535; INTERLEUKIN 6; INTERLEUKIN 8; PHOSPHATIDYLINOSITOL 3 KINASE; POLO LIKE KINASE INHIBITOR; PROTEIN BCL 6; PROTEIN KINASE B; UNCLASSIFIED DRUG; VOLASERTIB;

ADIPOSE DERIVED STEM CELL; ADULT; ARTICLE; B CELL LYMPHOMA; BREAST CANCER; BREAST CANCER CELL LINE; BREAST CARCINOGENESIS; CANCER GROWTH; CANCER RESISTANCE; CELL CONTACT; CELL FUNCTION; CELL INVASION; CELL ISOLATION; CELL MIGRATION; CELL PROLIFERATION; CELL SPECIFICITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; INTRAABDOMINAL FAT; INTRACELLULAR SIGNALING; MCF 7 CELL LINE; MDA MB-231 CELL LINE; MESENCHYMAL STEM CELL; SUBCUTANEOUS FAT; ADVERSE EFFECTS; BREAST TUMOR; CELL COMMUNICATION; COCULTURE; CYTOLOGY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; INDIRECT FLUORESCENT ANTIBODY TECHNIQUE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADULT; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL COMMUNICATION; COCULTURE TECHNIQUES; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HUMANS; IMMUNOHISTOCHEMISTRY; INTRA-ABDOMINAL FAT; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; REAL-TIME POLYMERASE CHAIN REACTION; SUBCUTANEOUS FAT;

EID: 84946572315     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5922     Document Type: Article

References (64)

1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. International journal of cancer Journal international du cancer. 2015; 136(5):E359-386.
2. Hanahan D and Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer cell. 2012; 21:309-322.
3. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S and Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999; 284:143-147.
4. Harasymiak-Krzyzanowska I, Niedojadlo A, Karwat J, Kotula L, Gil-Kulik P, Sawiuk M and Kocki J. Adipose tissue-derived stem cells show considerable promise for regenerative medicine applications. Cellular & molecular biology letters. 2013; 18:479-493.
5. Calis M, Demirtas TT, Atilla P, Tatar I, Ersoy O, Irmak G, Celik HH, Cakar AN, Gumusderelioglu M and Ozgur F. Estrogen as a novel agent for induction of adipose-derived mesenchymal stem cells for osteogenic differentiation: in vivo bone tissue-engineering study. Plastic and reconstructive surgery. 2014; 133:499e-510e.
6. Donnenberg VS, Zimmerlin L, Rubin JP and Donnenberg AD. Regenerative therapy after cancer: what are the risks? Tissue engineering Part B, Reviews. 2010; 16:567-575.
7. Freese KE, Kokai L, Edwards RP, Philips BJ, Sheikh MA, Kelley J, Comerci J, Marra KG, Rubin JP and Linkov F. Adipose-derived stems cells and their role in human cancer development, growth, progression, and metastasis: a systematic review. Cancer Res. 2015; 75:1161-1168.
8. Chandler EM, Seo BR, Califano JP, Andresen Eguiluz RC, Lee JS, Yoon CJ, Tims DT, Wang JX, Cheng L, Mohanan S, Buckley MR, Cohen I, Nikitin AY, Williams RM, Gourdon D, Reinhart-King CA, et al. Implanted adipose progenitor cells as physicochemical regulators of breast cancer. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109:9786-9791.
9. Cousin B, Ravet E, Poglio S, De Toni F, Bertuzzi M, Lulka H, Touil I, Andre M, Grolleau JL, Peron JM, Chavoin JP, Bourin P, Penicaud L, Casteilla L, Buscail L and Cordelier P. Adult stromal cells derived from human adipose tissue provoke pancreatic cancer cell death both in vitro and in vivo. PLoS One. 2009; 4:e6278.
10. Ryu H, Oh JE, Rhee KJ, Baik SK, Kim J, Kang SJ, Sohn JH, Choi E, Shin HC, Kim YM, Kim HS, Bae KS and Eom YW. Adipose tissue-derived mesenchymal stem cells cultured at high density express IFN-beta and suppress the growth of MCF-7 human breast cancer cells. Cancer Lett. 2014; 352:220-227.
11. Baglioni S, Francalanci M, Squecco R, Lombardi A, Cantini G, Angeli R, Gelmini S, Guasti D, Benvenuti S, Annunziato F, Bani D, Liotta F, Francini F, Perigli G, Serio M and Luconi M. Characterization of human adult stemcell populations isolated from visceral and subcutaneous adipose tissue. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2009; 23:3494-3505.
12. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D and Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006; 8:315-317.
13. Ranganath SH, Levy O, Inamdar MS and Karp JM. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell stem cell. 2012; 10:244-258.
14. Huang W, Chen Z, Zhang L, Tian D, Wang D, Fan D, Wu K and Xia L. Interleukin-8 Induces Expression of FOXC1 to Promote Trans-activation of CXCR1 and CCL2 in Hepatocellular Carcinoma Cell Lines and Formation of Metastases in Mice. Gastroenterology. 2015;149:1053-1067.
15. Choi SA, Lee YE, Kwak PA, Lee JY, Kim SS, Lee SJ, Phi JH, Wang KC, Song J, Song SH, Joo KM and Kim SK. Clinically applicable human adipose tissue-derived mesenchymal stem cells delivering therapeutic genes to brainstem gliomas. Cancer gene therapy. 2015; 22:302-311.
16. Subik K, Lee JF, Baxter L, Strzepek T, Costello D, Crowley P, Xing L, Hung MC, Bonfiglio T, Hicks DG and Tang P. The Expression Patterns of ER, PR, HER2, CK5/6, EGFR, Ki-67 and AR by Immunohistochemical Analysis in Breast Cancer Cell Lines. Breast cancer: basic and clinical research. 2010; 4:35-41.
17. Wei HJ, Zeng R, Lu JH, Lai WF, Chen WH, Liu HY, Chang YT and Deng WP. Adipose-derived stem cells promote tumor initiation and accelerate tumor growth by interleukin-6 production. Oncotarget. 2015; 6:7713-7726.
18. Albagli-Curiel O. Ambivalent role of BCL6 in cell survival and transformation. Oncogene. 2003; 22:507-516.
19. Waugh DJ and Wilson C. The interleukin-8 pathway in cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2008; 14:6735-6741.
20. Tsai JH and Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes & development. 2013; 27:2192-2206.
21. Evdokimova V, Tognon C, Ng T and Sorensen PH. Reduced proliferation and enhanced migration: two sides of the same coin? Molecular mechanisms of metastatic progression by YB-1. Cell cycle. 2009; 8:2901-2906.
22. Tsai JH, Donaher JL, Murphy DA, Chau S and Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer cell. 2012; 22:725-736.
23. Lamouille S, Xu J and Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nature reviews Molecular cell biology. 2014; 15:178-196.
24. Arcaro A and Wymann MP. Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem J. 1993; 296 :297-301.
25. Alessi DR, Cuenda A, Cohen P, Dudley DT and Saltiel AR. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem. 1995; 270:27489-27494.
26. Ritter A, Sanhaji M, Friemel A, Roth S, Rolle U, Louwen F and Yuan J. Functional analysis of phosphorylation of the mitotic centromere-associated kinesin by Aurora B kinase in human tumor cells. Cell cycle. 2015:0.
27. Polyak K and Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nature reviews Cancer. 2009; 9:265-273.
28. Lobba AR, Forni MF, Carreira AC and Sogayar MC. Differential expression of CD90 and CD14 stem cell markers in malignant breast cancer cell lines. Cytometry Part A: the journal of the International Society for Analytical Cytology. 2012; 81:1084-1091.
29. Gao ZW, Dong K and Zhang HZ. The roles of CD73 in cancer. BioMed research international. 2014; 2014:460654.
30. Mitra A, Mishra L and Li S. EMT, CTCs and CSCs in tumor relapse and drug-resistance. Oncotarget. 2015; 6:10697-10711.
31. Sanhaji M, Kreis NN, Zimmer B, Berg T, Louwen F and Yuan J. p53 is not directly relevant to the response of Pololike kinase 1 inhibitors. Cell cycle. 2012; 11:543-553.
32. Kreis NN, Louwen F, Zimmer B and Yuan J. Loss of p21Cip1/CDKN1A renders cancer cells susceptible to Pololike kinase 1 inhibition. Oncotarget. 2015; 6:6611-6626.
33. Yang Y, Bucan V, Baehre H, von der Ohe J, Otte A and Hass R. Acquisition of new tumor cell properties by MSCderived exosomes. Int J Oncol. 2015; 47:244-252.
34. Orecchioni S, Gregato G, Martin-Padura I, Reggiani F, Braidotti P, Mancuso P, Calleri A, Quarna J, Marighetti P, Aldeni C, Pruneri G, Martella S, Manconi A, Petit JY, Rietjens M and Bertolini F. Complementary populations of human adipose CD34+ progenitor cells promote growth, angiogenesis, and metastasis of breast cancer. Cancer Res. 2013; 73:5880-5891.
35. Zhao M, Sachs PC, Wang X, Dumur CI, Idowu MO, Robila V, Francis MP, Ware J, Beckman M, Rizki A, Holt SE and Elmore LW. Mesenchymal stem cells in mammary adipose tissue stimulate progression of breast cancer resembling the basal-type. Cancer biology & therapy. 2012; 13:782-792.
36. Muehlberg FL, Song YH, Krohn A, Pinilla SP, Droll LH, Leng X, Seidensticker M, Ricke J, Altman AM, Devarajan E, Liu W, Arlinghaus RB and Alt EU. Tissue-resident stem cells promote breast cancer growth and metastasis. Carcinogenesis. 2009; 30:589-597.
37. Qiao L, Xu ZL, Zhao TJ, Ye LH and Zhang XD. Dkk-1 secreted by mesenchymal stem cells inhibits growth of breast cancer cells via depression of Wnt signalling. Cancer Lett. 2008; 269:67-77.
38. Sun B, Roh KH, Park JR, Lee SR, Park SB, Jung JW, Kang SK, Lee YS and Kang KS. Therapeutic potential of mesenchymal stromal cells in a mouse breast cancer metastasis model. Cytotherapy. 2009; 11:289-298, 281 p following 298.
39. Chau YY, Bandiera R, Serrels A, Martinez-Estrada OM, Qing W, Lee M, Slight J, Thornburn A, Berry R, McHaffie S, Stimson RH, Walker BR, Chapuli RM, Schedl A and Hastie N. Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source. Nat Cell Biol. 2014; 16:367-+.
40. Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obesity reviews: an official journal of the International Association for the Study of Obesity. 2010; 11:11-18.
41. Schweizer R, Tsuji W, Gorantla VS, Marra KG, Rubin JP and Plock JA. The role of adipose-derived stem cells in breast cancer progression and metastasis. Stem cells international. 2015; 2015:120949.
42. Wang Y, Xu RC, Zhang XL, Niu XL, Qu Y, Li LZ and Meng XY. Interleukin-8 secretion by ovarian cancer cells increases anchorage-independent growth, proliferation, angiogenic potential, adhesion and invasion. Cytokine. 2012; 59:145-155.
43. Chou CH, Lai SL, Chen CN, Lee PH, Peng FC, Kuo ML and Lai HS. IL-6 regulates Mcl-1L expression through the JAK/PI3K/Akt/CREB signaling pathway in hepatocytes: implication of an anti-apoptotic role during liver regeneration. PLoS One. 2013; 8:e66268.
44. Jamdade VS, Sethi N, Mundhe NA, Kumar P, Lahkar M and Sinha N. Therapeutic Targets of Triple Negative Breast Cancer: A Review. British journal of pharmacology. 2015; 172:4228-37.
45. Pallua N, Serin M and Wolter TP. Characterisation of angiogenetic growth factor production in adipose tissuederived mesenchymal cells. Journal of plastic surgery and hand surgery. 2014; 48:412-416.
46. Lin R, Wang S and Zhao RC. Exosomes from human adipose-derived mesenchymal stem cells promote migration through Wnt signaling pathway in a breast cancer cell model. Molecular and cellular biochemistry. 2013; 383:13-20.
47. Yu JM, Sun W, Hua F, Xie J, Lin H, Zhou DD and Hu ZW. BCL6 induces EMT by promoting the ZEB1-mediated transcription repression of E-cadherin in breast cancer cells. Cancer Lett. 2015; 365:190-200.
48. Xie G, Yao Q, Liu Y, Du S, Liu A, Guo Z, Sun A, Ruan J, Chen L, Ye C and Yuan Y. IL-6-induced epithelialmesenchymal transition promotes the generation of breast cancer stem-like cells analogous to mammosphere cultures. Int J Oncol. 2012; 40:1171-1179.
49. Yin J, Zeng F, Wu N, Kang K, Yang Z and Yang H. Interleukin-8 promotes human ovarian cancer cell migration by epithelial-mesenchymal transition induction in vitro. Clinical & translational oncology: official publication of the Federation of Spanish Oncology Societies and of the National Cancer Institute of Mexico. 2015; 17:365-370.
50. Liu CY, Xu JY, Shi XY, Huang W, Ruan TY, Xie P and Ding JL. M2-polarized tumor-associated macrophages promoted epithelial-mesenchymal transition in pancreatic cancer cells, partially through TLR4/IL-10 signaling pathway. Laboratory investigation; a journal of technical methods and pathology. 2013; 93:844-854.
51. Crotty S, Johnston RJ and Schoenberger SP. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nature immunology. 2010; 11:114-120.
52. Walker SR, Liu S, Xiang M, Nicolais M, Hatzi K, Giannopoulou E, Elemento O, Cerchietti L, Melnick A and Frank DA. The transcriptional modulator BCL6 as a molecular target for breast cancer therapy. Oncogene. 2015; 34:1073-1082.
53. Tao D, Pan Y, Jiang G, Lu H, Zheng S, Lin H and Cao F. B-Myb regulates snail expression to promote epithelial-tomesenchymal transition and invasion of breast cancer cell. Medical oncology. 2015; 32:412.
54. Liu L, Zhang J, Fang C, Zhang Z, Feng Y and Xi X. OCT4 mediates FSH-induced epithelial-mesenchymal transition and invasion through the ERK1/2 signaling pathway in epithelial ovarian cancer. Biochemical and biophysical research communications. 2015; 461:525-532.
55. Chen X, Ye S, Xiao W, Wang W, Luo L and Liu Y. ERK1/2 pathway mediates epithelial-mesenchymal transition by cross-interacting with TGFbeta/Smad and Jagged/Notch signaling pathways in lens epithelial cells. International journal of molecular medicine. 2014; 33:1664-1670.
56. Holohan C, Van Schaeybroeck S, Longley DB and Johnston PG. Cancer drug resistance: an evolving paradigm. Nature reviews Cancer. 2013; 13:714-726.
57. Schmidt JM, Panzilius E, Bartsch HS, Irmler M, Beckers J, Kari V, Linnemann JR, Dragoi D, Hirschi B, Kloos UJ, Sass S, Theis F, Kahlert S, Johnsen SA, Sotlar K and Scheel CH. Stem-cell-like properties and epithelial plasticity arise as stable traits after transient Twist1 activation. Cell reports. 2015; 10:131-139.
58. Ng LW, Yip SK, Wong HK, Yam GH, Liu YM, Lui WT, Wang CC and Choy KW. Adipose-derived stem cells from pregnant women show higher proliferation rate unrelated to estrogen. Human reproduction. 2009; 24:1164-1170.
59. Kreis NN, Sommer K, Sanhaji M, Kramer A, Matthess Y, Kaufmann M, Strebhardt K and Yuan J. Long-term downregulation of Polo-like kinase 1 increases the cyclindependent kinase inhibitor p21(WAF1/CIP1). Cell cycle. 2009; 8:460-472.
60. Muschol-Steinmetz C, Friemel A, Kreis NN, Reinhard J, Yuan J and Louwen F. Function of survivin in trophoblastic cells of the placenta. PLoS One. 2013; 8:e73337.
61. Sanhaji M, Friel CT, Kreis NN, Kramer A, Martin C, Howard J, Strebhardt K and Yuan J. Functional and spatial regulation of mitotic centromere-associated kinesin by cyclin-dependent kinase 1. Molecular and cellular biology. 2010; 30:2594-2607.
62. Sanhaji M, Ritter A, Belsham HR, Friel CT, Roth S, Louwen F and Yuan J. Polo-like kinase 1 regulates the stability of the mitotic centromere-associated kinesin in mitosis. Oncotarget. 2014; 5:3130-3144.
63. Ritter A, Sanhaji M, Steinhauser K, Roth S, Louwen F and Yuan J. The activity regulation of the mitotic centromereassociated kinesin by Polo-like kinase 1. Oncotarget. 2015; 6:6641-6655.
64. Louwen F, Muschol-Steinmetz C, Friemel A, Kampf AK, Tottel E, Reinhard J and Yuan J. Targeted gene analysis: increased B-cell lymphoma 6 in preeclamptic placentas. Human pathology. 2014; 45:1234-1242.