Adipose‑derived mesenchymal stem cells exhibit tumor tropism and promote tumorsphere formation of breast cancer cells
- Authors:
- Yanqing Chen
- Yunfan He
- Xuecen Wang
- Feng Lu
- Jianhua Gao
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Affiliations: Department of Plastic and Cosmetic Surgery, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong 510515, P.R. China - Published online on: February 15, 2019 https://doi.org/10.3892/or.2019.7018
- Pages: 2126-2136
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Copyright: © Chen et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
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Nelson HD, Zakher B, Cantor A, Fu R, Griffin J, O'Meara ES, Buist DS, Kerlikowske K, van Ravesteyn NT, Trentham-Dietz A, et al: Risk factors for breast cancer for women aged 40 to 49 years: A systematic review and meta-analysis. Ann Intern Med. 156:635–648. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Porter PL: Global trends in breast cancer incidence and mortality. Salud Publica Mex. 51 (Suppl 2):S141–S146. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
McGuire KP, Eisen S, Rodriguez A, Meade T, Cox CE and Khakpour N: Factors associated with improved outcome after surgery in metastatic breast cancer patients. Am J Surg. 198:511–515. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Munhoz AM, Montag E, Filassi JR and Gemperli R: Current approaches to managing partial breast defects: The role of conservative breast surgery reconstruction. Anticancer Res. 34:1099–1114. 2014.PubMed/NCBI | |
|
Longaker MT, Aston SJ, Baker DC and Rohrich RJ: Fat Transfer in 2014: What we do not know. Plast Reconstr Surg. 133:1305–1307. 2014.PubMed/NCBI | |
|
Eto H, Kato H, Suga H, Aoi N, Doi K, Kuno S and Yoshimura K: The Fate of Adipocytes after nonvascularized fat grafting. Plast Reconstr Surg. 129:1081–1092. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Chung MT, Paik KJ, Atashroo DA, Hyun JS, McArdle A, Senarath-Yapa K, Zielins ER, Tevlin R, Duldulao C, Hu MS, et al: Studies in fat grafting: Part I. Effects of injection technique on in vitro fat viability and in vivo volume retention. Plast Reconstr Surg. 134:29–38. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Atashroo D, Raphel J, Chung MT, Paik KJ, Parisi-Amon A, McArdle A, Senarath-Yapa K, Zielins ER, Tevlin R, Duldulao C, et al: Studies in fat grafting: Part II. Effects of injection mechanics on material properties of fat. Plast Reconstr Surg. 134:39–46. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Dong Z, Peng Z, Chang Q, Zhan W, Zeng Z, Zhang S and Lu F: The angiogenic and adipogenic modes of adipose tissue after free fat grafting. Plast Reconstr Surg. 135:556e–567e. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Bellei B, Migliano E, Tedesco M, Caputo S, Papaccio F, Lopez G and Picardo M: Adipose tissue-derived extracellular fraction characterization: Biological and clinical considerations in regenerative medicine. Stem Cell Res Ther. 9:2072018. View Article : Google Scholar : PubMed/NCBI | |
|
Yoshimura K, Shigeura T, Matsumoto D, Sato T, Takaki Y, Aiba-Kojima E, Sato K, Inoue K, Nagase T, Koshima I, et al: Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J Cell Physiol. 208:64–76. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Pearl RA, Leedham SJ and Pacifico MD: The safety of autologous fat transfer in breast cancer: Lessons from stem cell biology. J Plast Reconstr Aesthet Surg. 65:283–288. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y, Lehuédé C, Laurent V, Dirat B, Dauvillier S, Bochet L, Le Gonidec S, Escourrou G, Valet P and Muller C: Adipose tissue and breast epithelial cells: A dangerous dynamic duo in breast cancer. Cancer Lett. 324:142–151. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Kolle SF, Fischer-Nielsen A, Mathiasen AB, Elberg JJ, Oliveri RS, Glovinski PV, Kastrup J, Kirchhoff M, Rasmussen BS, Talman ML, et al: Enrichment of autologous fat grafts with ex-vivo expanded adipose tissue-derived stem cells for graft survival: A randomised placebo-controlled trial. Lancet. 382:1113–1120. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Doi K, Ogata F, Eto H, Kato H, Kuno S, Kinoshita K, Kanayama K, Feng J, Manabe I and Yoshimura K: Differential contributions of graft-derived and host-derived cells in tissue regeneration/remodeling after fat grafting. Plast Reconstr Surg. 135:1607–1617. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Suga H, Eto H, Aoi N, Kato H, Araki J, Doi K, Higashino T and Yoshimura K: Adipose tissue remodeling under ischemia: Death of adipocytes and activation of stem/progenitor cells. Plast Reconstr Surg. 126:1911–1923. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Kuhbier JW, Bucan V, Reimers K, Strauss S, Lazaridis A, Jahn S, Radtke C and Vogt PM: Observed changes in the morphology and phenotype of breast cancer cells in direct co-culture with adipose-derived stem cells. Plast Reconstr Surg. 134:414–423. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Kamat P, Schweizer R, Kaenel P, Salemi S, Calcagni M, Giovanoli P, Gorantla VS, Eberli D, Andres AC and Plock JA: Human adipose-derived mesenchymal stromal cells may promote breast cancer progression and metastatic spread. Plast Reconstr Surg. 136:76–84. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Kucerova L, Skolekova S, Matuskova M, Bohac M and Kozovska Z: Altered features and increased chemosensitivity of human breast cancer cells mediated by adipose tissue-derived mesenchymal stromal cells. Bmc Cancer. 13:5352013. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Y, Daquinag A, Traktuev DO, Amaya-Manzanares F, Simmons PJ, March KL, Pasqualini R, Arap W and Kolonin MG: White adipose tissue cells are recruited by experimental tumors and promote cancer progression in mouse models. Cancer Res. 69:5259–5266. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Eterno V, Zambelli A, Pavesi L, Villani L, Zanini V, Petrolo G, Manera S, Tuscano A and Amato A: Adipose-derived mesenchymal stem cells (ASCs) may favour breast cancer recurrence via HGF/c-Met signaling. Oncotarget. 5:613–633. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Alessio N, Bohn W, Rauchberger V, Rizzolio F, Cipollaro M, Rosemann M, Irmler M, Beckers J, Giordano A and Galderisi U: Silencing of RB1 but not of RB2/P130 induces cellular senescence and impairs the differentiation potential of human mesenchymal stem cells. Cell Mol Life Sci. 70:1637–1651. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Gary RK and Kindell SM: Quantitative assay of senescence-associated beta-galactosidase activity in mammalian cell extracts. Anal Biochem. 343:329–334. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Wang W, Zhong W, Yuan J, Yan C, Hu S, Tong Y, Mao Y, Hu T, Zhang B and Song G: Involvement of Wnt/β-catenin signaling in the mesenchymal stem cells promote metastatic growth and chemoresistance of cholangiocarcinoma. Oncotarget. 6:42276–42289. 2015.PubMed/NCBI | |
|
Zhou M, Liu S, Jiang Y, Ma H, Shi M, Wang Q, Zhong W, Liao W and Xing MM: Doxorubicin-loaded single wall nanotube thermo-sensitive hydrogel for gastric cancer chemo-photothermal therapy. Adv Funct Mater. 25:4730–4739. 2015. View Article : Google Scholar | |
|
Naito S, von Eschenbach AC, Giavazzi R and Fidler IJ: Growth and metastasis of tumor cells isolated from a human renal cell carcinoma implanted into different organs of nude mice. Cancer Res. 46:4109–4115. 1986.PubMed/NCBI | |
|
Choi JS, Kim BS, Kim JY, Kim JD, Choi YC, Yang HJ, Park K, Lee HY and Cho YW: Decellularized extracellular matrix derived from human adipose tissue as a potential scaffold for allograft tissue engineering. J Biomed Mater Res A. 97:292–299. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Rhee K, Lee J and Eom Y: Mesenchymal stem cell-mediated effects of tumor support or suppression. Int J Mol Sci. 16:30015–30033. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Waked K, Colle J, Doornaert M, Cocquyt V and Blondeel P: Systematic review: The oncological safety of adipose fat transfer after breast cancer surgery. Breast. 31:128–136. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Massa M, Gasparini S, Baldelli I, Scarabelli L, Santi P, Quarto R and Repaci E: Interaction between breast cancer cells and adipose tissue cells derived from fat grafting. Aesthet Surg J. 36:358–363. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Ito S, Kai Y, Masuda T, Tanaka F, Matsumoto T, Kamohara Y, Hayakawa H, Ueo H, Iwaguro H, Hedrick MH, et al: Long-term outcome of adipose-derived regenerative cell-enriched autologous fat transplantation for reconstruction after breast-conserving surgery for Japanese women with breast cancer. Surg Today. 47:1500–1511. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Bielli A, Scioli MG, Gentile P, Agostinelli S, Tarquini C, Cervelli V and Orlandi A: Adult adipose-derived stem cells and breast cancer: A controversial relationship. Springerplus. 3:1–10. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Ponte AL, Marais E, Gallay N, Langonne A, Delorme B, Herault O, Charbord P and Domenech J: The in vitro migration capacity of human bone marrow mesenchymal stem cells: Comparison of chemokine and growth factor chemotactic activities. Stem Cells. 25:1737–1745. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Spaeth E, Klopp A, Dembinski J, Andreeff M and Marini F: Inflammation and tumor microenvironments: Defining the migratory itinerary of mesenchymal stem cells. Gene Ther. 15:730–738. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Lejmi E, Perriraz N, Clément S, Morel P, Baertschiger R, Christofilopoulos P, Meier R, Bosco D, Bühler LH and Gonelle-Gispert C: Inflammatory chemokines MIP-1δ and MIP-3α are involved in the migration of multipotent mesenchymal stromal cells induced by hepatoma cells. Stem Cells Dev. 24:1223–1235. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Chamberlain G, Smith H, Rainger GE and Middleton J: Mesenchymal stem cells exhibit firm adhesion, crawling, spreading and transmigration across aortic endothelial cells: Effects of chemokines and shear. PLoS One. 6:e256632011. View Article : Google Scholar : PubMed/NCBI | |
|
Wang H, Cao F, De A, Cao Y, Contag C, Gambhir SS, Wu JC and Chen X: Trafficking mesenchymal stem cell engraftment and differentiation in tumor-bearing mice by bioluminescence imaging. Stem Cells. 27:1548–1558. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Menon LG, Picinich S, Koneru R, Gao H, Lin SY, Koneru M, Mayer-Kuckuk P, Glod J and Banerjee D: Differential gene expression associated with migration of mesenchymal stem cells to conditioned medium from tumor cells or bone marrow cells. Stem Cells. 25:520–528. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Ho IA, Chan KY, Ng WH, Guo CM, Hui KM, Cheang P and Lam PY: Matrix metalloproteinase 1 is necessary for the migration of human bone marrow-derived mesenchymal stem cells toward human glioma. Stem Cells. 27:1366–1375. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Egea V, von Baumgarten L, Schichor C, Berninger B, Popp T, Neth P, Goldbrunner R, Kienast Y, Winkler F, Jochum M, et al: TNF-α respecifies human mesenchymal stem cells to a neural fate and promotes migration toward experimental glioma. Cell Death Differ. 18:853–863. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Dwyer RM, Potter-Beirne SM, Harrington KA, Lowery AJ, Hennessy E, Murphy JM, Barry FP, O'Brien T and Kerin MJ: Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res. 13:5020–5027. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Lazennec G and Richmond A: Chemokines and chemokine receptors: New insights into cancer-related inflammation. Trends Mol Med. 16:133–144. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Balkwill F: Cancer and the chemokine network. Nat Rev Cancer. 4:540–550. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Zernecke A, Weber KS, Erwig LP, Kluth DC, Schroppel B, Rees AJ and Weber C: Combinatorial model of chemokine involvement in glomerular monocyte recruitment: Role of CXC chemokine receptor 2 in infiltration during nephrotoxic nephritis. J Immunol. 166:5755–5762. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Ali S and Lazennec G: Chemokines: Novel targets for breast cancer metastasis. Cancer Metastasis Rev. 26:401–420. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Zlotnik A, Burkhardt AM and Homey B: Homeostatic chemokine receptors and organ-specific metastasis. Nat Rev Immunol. 11:597–606. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Escobar P, Bouclier C, Serret J, Bieche I, Brigitte M, Caicedo A, Sanchez E, Vacher S, Vignais ML, Bourin P, et al: IL-1β produced by aggressive breast cancer cells is one of the factors that dictate their interactions with mesenchymal stem cells through chemokine production. Oncotarget. 6:29034–29047. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Griffith JW, Sokol CL and Luster AD: Chemokines and chemokine receptors: Positioning cells for host defense and immunity. Annu Rev Immunol. 32:659–702. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Li Y, Wu J, Zhang W, Zhang N and Guo H: Identification of serum CCL15 in hepatocellular carcinoma. Br J Cancer. 108:99–106. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Cao L, Zhou Y, Zhai B, Liao J, Xu W, Zhang R, Li J, Zhang Y, Chen L, Qian H, et al: Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines. BMC Gastroenterol. 11:712011. View Article : Google Scholar : PubMed/NCBI | |
|
Weiswald L, Bellet D and Dangles-Marie V: Spherical cancer models in tumor biology. Neoplasia. 17:1–15. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Pastrana E, Silva-Vargas V and Doetsch F: Eyes wide open: A critical review of sphere-formation as an assay for stem cells. Cell Stem Cell. 8:486–498. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA and Daidone MG: Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 65:5506–5511. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Liu A, Yu X and Liu S: Pluripotency transcription factors and cancer stem cells: Small genes make a big difference. Chin J Cancer. 32:483–487. 2013.PubMed/NCBI | |
|
Santini R, Pietrobono S, Pandolfi S, Montagnani V, D'Amico M, Penachioni JY, Vinci MC, Borgognoni L and Stecca B: SOX2 regulates self-renewal and tumorigenicity of human melanoma-initiating cells. Oncogene. 33:4697–4708. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Turhan AG, Lemoine FM, Debert C, Bonnet ML, Baillou C, Picard F, Macintyre EA and Varet B: Highly purified primitive hematopoietic stem cells are PML-RARA negative and generate nonclonal progenitors in acute promyelocytic leukemia. Blood. 85:2154–2161. 1995.PubMed/NCBI | |
|
Holyoake TL, Jiang X, Drummond MW, Eaves AC and Eaves CJ: Elucidating critical mechanisms of deregulated stem cell turnover in the chronic phase of chronic myeloid leukemia. Leukemia. 16:549–558. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Marsden CG, Wright MJ, Pochampally R and Rowan BG: Breast tumor-initiating cells isolated from patient core biopsies for study of hormone action. Methods Mol Biol. 590:363–375. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C and De Maria R: Identification and expansion of human colon-cancer-initiating cells. Nature. 445:111–115. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al: The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 133:704–715. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Thiery JP and Sleeman JP: Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol. 7:131–142. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Kalluri R and Weinberg RA: The basics of epithelial-mesenchymal transition. J Clin Invest. 119:1420–1428. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Vega SL, Kwon MY and Burdick JA: Recent advances in hydrogels for cartilage tissue engineering. Eur Cell Mater. 33:59–75. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Kondiah PJ, Choonara YE, Kondiah PP, Marimuthu T, Kumar P, du Toit LC and Pillay V: A review of injectable polymeric hydrogel systems for application in bone tissue engineering. Molecules. 21(pii): E15802016. View Article : Google Scholar : PubMed/NCBI | |
|
Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP and Hedrick MH: Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng. 7:211–228. 2001. View Article : Google Scholar : PubMed/NCBI |
