Optimum 3D matrix stiffness for maintenance of cancer stem cells is dependent on tissue origin of cancer cells

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Jabbari, Esmaiel ^a   Sarvestani, Samaneh K ^a   Daneshian, Leily ^a   Moeinzadeh, Seyedsina ^a  

^a The Department of Mechanical Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACRYLIC ACID DERIVATIVE; BREAST CANCER RESISTANCE PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; MESSENGER RNA; POLYETHYLENE GLYCOL DIACRYLATE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TAZ; TRANSCRIPTION FACTOR YAP; UNCLASSIFIED DRUG; UVOMORULIN; HYDROGEL; MACROGOL DERIVATIVE; POLY(ETHYLENE GLYCOL)DIACRYLATE;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER STEM CELL; CELL COUNT; CELL DENSITY; CELL ENCAPSULATION; CELL GROWTH; CELL LINEAGE; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GASTRIC CANCER CELL LINE; HCT116 CELL LINE; HUMAN; HUMAN CELL; HYDROGEL; MCF 7 CELL LINE; MICROENVIRONMENT; OSTEOSARCOMA CELL; PROTEIN EXPRESSION; TUMOR SEEDING; TUMOR VOLUME; FLOW CYTOMETRY; HCT 116 CELL LINE; IMMUNOBLOTTING; MCF-7 CELL LINE; OSTEOSARCOMA; PATHOPHYSIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; STOMACH TUMOR; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

CELL COUNT; CELL LINE, TUMOR; FLOW CYTOMETRY; HCT116 CELLS; HUMANS; HYDROGEL; IMMUNOBLOTTING; MCF-7 CELLS; NEOPLASTIC STEM CELLS; OSTEOSARCOMA; POLYETHYLENE GLYCOLS; REAL-TIME POLYMERASE CHAIN REACTION; STOMACH NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84940777013     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132377     Document Type: Article

References (66)

1. Tobin NP, Harrell JC, Lovrot J, Egyhazi Brage S, Frostvik-Stolt M, Ferno M, et al. (2015) The molecular subtype and tumor characteristics of breast cancer metastases significantly influence patient post-relapse survival. Ann Oncol 26: 81-88. doi: 10.1093/annonc/mdu498 PMID: 25361981
2. Fenner A (2012) Prostate cancer: Hypoxia predicts relapse and recurrence after radiotherapy. Nat Rev Urol 9: 237.
3. Stokes ME, Thompson D, Montoya EL, Weinstein MC, Winer EP, Earle CC (2008) Ten-year survival and cost following breast cancer recurrence: Estimates from seer-medicare data. Value Health 11: 213-20. doi: 10.1111/j.1524-4733.2007.00226.x PMID: 18380633
4. Tsai WS, Hsieh PS, Yeh CY, Chiang JM, Tang R, Chen JS, et al. (2011) Long-term survival benefits of adjuvant chemotherapy by decreasing incidence of tumor recurrence without delaying relapse in stage III colorectal cancer. Int J Colorectal Dis 26: 1329-38. doi: 10.1007/s00384-011-1214-8 PMID: 21556841
5. Pattabiraman DR, Weinberg RA (2014) Tackling the cancer stem cells - what challenges do they pose? Nature Rev Drug Discov 13: 497-512.
6. Liu TJ, Sun BC, Zhao XL, Zhao XM, Sun T, Gu Q, et al. (2013) CD133+ cells with cancer stem cell characteristics associates with vasculogenic mimicry in triple-negative breast cancer. Oncogene 32: 544-53. doi: 10.1038/onc.2012.85 PMID: 22469978
7. Fang Y, Xiang J, Chen Z, Gu X, Li Z, Tang F, et al. (2012) miRNA expression profile of colon cancer stem cells compared to non-stem cells using the SW1116 cell line. Oncol Rep 28: 2115-24. doi: 10.3892/or.2012.2054 PMID: 23007737
8. Fessler E, Dijkgraaf FE, De Sousa EMF, Medema JP (2013) Cancer stem cell dynamics in tumor progression and metastasis: Is the microenvironment to blame? Cancer Lett 341: 97-104. doi: 10.1016/j.canlet.2012.10.015 PMID: 23089245
9. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689. PMID: 16923388
10. Pek YS, Wan ACA, Ying JY (2010) The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel. Biomaterials 31: 385-391. doi: 10.1016/j.biomaterials.2009.09.057 PMID: 19811817
11. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-54. PMID: 16169468
12. Baker EL, Lu J, Yu DH, Bonnecaze RT, Zaman MH (2010) Cancer cell stiffness: Integrated roles of three-dimensional matrix stiffness and transforming potential. Biophys J 99: 2048-2057. doi: 10.1016/j.bpj.2010.07.051 PMID: 20923638
13. Jamal M, Rath BH, Tsang PS, Camphausen K, Tofilon PJ (2012) The brain microenvironment preferentially enhances the radioresistance of CD133(+) glioblastoma stem-like cells. Neoplasia 14: 150-158. PMID: 22431923
14. Chen L, Xiao Z, Meng Y, Zhao Y, Han J, Su G, et al. (2012) The enhancement of cancer stem cell properties of MCF-7 cells in 3D collagen scaffolds for modeling of cancer and anti-cancer drugs. Biomaterials 33: 1437-1444. doi: 10.1016/j.biomaterials.2011.10.056 PMID: 22078807
15. Hale NA, Yang Y, Rajagopalan P (2010) Cell migration at the interface of a dual chemical-mechanical gradient. ACS Appl Mater Interf 2: 2317-2324.
16. Yang X, Sarvestani SK, Moeinzadeh S, He X, Jabbari E (2013) Three-dimensional-engineered matrix to study cancer stem cells and tumorsphere formation: Effect of matrix modulus. Tissue Eng Part A 19: 669-84. doi: 10.1089/ten.TEA.2012.0333 PMID: 23013450
17. Yang X, Sarvestani SK, Moeinzadeh S, He X, Jabbari E (2013) Effect of CD44 binding peptide conjugated to an engineered inert matrix on maintenance of breast cancer stem cells and tumorsphere formation. PLoS One 8: e59147. doi: 10.1371/journal.pone.0059147 PMID: 23527117
18. Tang X, Kuhlenschmidt TB, Zhou J, Bell P, Wang F, Kuhlenschmidt MS, et al. (2010) Mechanical force affects expression of an in vitro metastasis-like phenotype in HCT-8 cells. Biophys J 99: 2460-2469. doi: 10.1016/j.bpj.2010.08.034 PMID: 20959086
19. Mylona E, Dailiana ZH, Trepat X, Lagoudakis MG (2008) Substrate rigidity dictates phenotype, survival, and mechanics of primary human osteosarcoma cells. Eur Symp Biomed Eng 1-4.
20. He X, Ma J, Jabbari E (2008) Effect of grafting RGD and BMP-2 protein-derived peptides to a hydrogel substrate on osteogenic differentiation of marrow stromal cells. Langmuir 24: 12508-12516. doi: 10.1021/la802447v PMID: 18837524
21. Yu F, Li J, Chen H, Fu J, Ray S, Huang S, et al. (2011) Kruppel-like factor 4 (KLF4) is required for maintenance of breast cancer stem cells and for cell migration and invasion. Oncogene 30: 2161-2172. doi: 10.1038/onc.2010.591 PMID: 21242971
22. Yan J, Sun YH, Zhu H, Marcu L, Revzin A (2009) Enzyme-containing hydrogel micropatterns serving a dual purpose of cell sequestration and metabolite detection. Biosens Bioelectron 24: 2604-2610. doi: 10.1016/j.bios.2009.01.029 PMID: 19251408
23. He X, Yang X, Jabbari E (2012) Combined effect of osteopontin and BMP-2 derived peptides grafted to an adhesive hydrogel on osteogenic and vasculogenic differentiation of marrow stromal cells. Langmuir 28: 5387-5397. doi: 10.1021/la205005h PMID: 22372823
24. Henderson JA, He X, Jabbari E (2008) Concurrent differentiation of marrow stromal cells to osteogenic and vasculogenic lineages. Macromol Biosci 8: 499-507. doi: 10.1002/mabi.200800093 PMID: 17941111
25. Sun YR, Kong WQ, Falk A, Hu J, Zhou LF, Pollard S, et al. (2009) CD133 (prominin) negative human neural stem cells are clonogenic and tripotent. PLoS One 4: e5498. doi: 10.1371/journal.pone.0005498 PMID: 19430532
26. Abu-Ali S, Fotovati A, Shirasuna K (2008) Tyrosine-kinase inhibition results in EGFR clustering at focal adhesions and consequent exocytosis in upar down-regulated cells of head and neck cancers. Mol Cancer 7: 47. doi: 10.1186/1476-4598-7-47 PMID: 18519000
27. Meyer JS, Shearer RL, Capowski EE, Wright LS, Wallace KA, McMillan EL, et al. (2009) Modeling early retinal development with human embryonic and induced pluripotent stem cells. Proc Natl Acad Sci U S A 106: 16698-16703. doi: 10.1073/pnas.0905245106 PMID: 19706890
28. Xie SP, Macedo P, Hew M, Nassenstein C, Lee KY, Chung KF (2009) Expression of transforming growth factor-beta (TGF-beta) in chronic idiopathic cough. Respir Res 10: 40. doi: 10.1186/1465-9921-10-40 PMID: 19463161
29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative pcr and the 2(-delta delta c(t)) method. Methods 25: 402-8. PMID: 11846609
30. Lynn AD, Kyriakides TR, Bryant SJ (2010) Characterization of the in vitro macrophage response and in vivo host response to poly(ethylene glycol)-based hydrogels. J Biomed Mater Res Part A 93: 941-953.
31. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B Meth 57: 289-300.
32. Britton KM, Eyre R, Harvey IJ, Stemke-Hale K, Browell D, Lennard TW, et al. Breast cancer, side population cells and ABCG2 expression. Cancer Lett 323: 97-105. doi: 10.1016/j.canlet.2012.03.041 PMID: 22521545
33. Hiraga T, Ito S, Nakamura H (2011) Side population in MDA-MB-231 human breast cancer cells exhibits cancer stem cell-like properties without higher bone-metastatic potential. Oncol Rep 25: 289-296. PMID: 21109989
34. Subik K, Lee JF, Baxter L, Strzepek T, Costello D, Crowley P, et al. (2010) The expression patterns of ER, PR, HER2, Ck5/6, EGFR, Ki-67 and AR by immunohistochemical analysis in breast cancer cell lines. Breast Cancer Auckl 4: 35-41. PMID: 20697531
35. Ricardo S, Vieira AF, Gerhard R, Leitao D, Pinto R, Cameselle-Teijeiro JF, et al. (2011) Breast cancer stem cell markers CD44, CD24 and ALDH1: Expression distribution within intrinsic molecular subtype. J Clin Path 64: 937-946. doi: 10.1136/jcp.2011.090456 PMID: 21680574
36. Soofi SS, Last JA, Liliensiek SJ, Nealey PF, Murphy CJ (2009) The elastic modulus of matrigel (TM) as determined by atomic force microscopy. J Struct Biol 167: 216-219. doi: 10.1016/j.jsb.2009.05.005 PMID: 19481153
37. Louie E, Nik S, Chen JS, Schmidt M, Song B, Pacson C, et al. (2010) Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation. Breast Cancer Res 12: R94. doi: 10.1186/bcr2773 PMID: 21067584
38. Holliday DL, Speirs V (2011) Choosing the right cell line for breast cancer research. Breast Cancer Res 13: 215. doi: 10.1186/bcr2889 PMID: 21884641
39. Sakai K, Kurokawa T, Furui Y, Kuronuma Y, Sekiguchi M, Ando J, et al. (2011) Invasion of carcinoma cells into reconstituted type I collagen gels: Visual real-time analysis by time-lapse microscopy. Biosci Trends 5: 10-16. PMID: 21422595
40. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110. PMID: 17122772
41. Roy S, Majumdar AP (2012) Signaling in colon cancer stem cells. J Mol Signal 7: 11. doi: 10.1186/1750-2187-7-11 PMID: 22866952
42. Chen Z, Xu WR, Qian H, Zhu W, Bu XF, Wang S, et al. (2009) OCT4, a novel marker for human gastric cancer. J Surg Oncol 99: 414-419. doi: 10.1002/jso.21270 PMID: 19347886
43. Tirino V, Desiderio V, Paino F, De Rosa A, Papaccio F, Fazioli F, et al. (2011) Human primary bone sarcomas contain CD133+ cancer stem cells displaying high tumorigenicity in vivo. FASEB J 25: 2022-2030. doi: 10.1096/fj.10-179036 PMID: 21385990
44. Jaggupilli A, Elkord E (2012) Significance of CD44 and CD24 as cancer stem cell markers: An enduring ambiguity. Clin Dev Immunol 708036.
45. Hibino S, Shibuya M, Engbring JA, Mochizuki M, Nomizu M, Kleinman HK (2004) Identification of an active site on the laminin alpha 5 chain globular domain that binds to CD44 and inhibits malignancy. Cancer Res 64: 4810-4816. PMID: 15256450
46. Peppas NA, Barr-Howell BD (1986) Characterization of the cross-linked structure of hydrogels. Hydrogels in Medicine and Pharmacy 1: 27-56.
47. Flecha FLG, Levi V (2003) Determination of the molecular size of bsa by fluorescence anisotropy. Biochem Mol Biol Ed 31: 319-322.
48. Engberg K, Frank CW (2011) Protein diffusion in photopolymerized poly(ethylene glycol) hydrogel networks. Biomed Mater 6: 055006. doi: 10.1088/1748-6041/6/5/055006 PMID: 21873762
49. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, et al. (2011) Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 145: 926-40. doi: 10.1016/j.cell.2011.04.029 PMID: 21663795
50. Yamamoto M, Taguchi Y, Ito-Kureha T, Semba K, Yamaguchi N, Inoue J (2013) NF-kb non-cell-autonomously regulates cancer stem cell populations in the basal-like breast cancer subtype. Nature Commun 4: 2299.
51. Lu J, Ye XC, Fan F, Xia L, Bhattacharya R, Bellister S, et al. (2013) Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of jagged-1. Cancer Cell 23: 171-185. doi: 10.1016/j.ccr.2012.12.021 PMID: 23375636
52. Fillmore CM, Gupta PB, Rudnick JA, Caballero S, Keller PJ, Lander ES, et al. (2010) Estrogen expands breast cancer stem-like cells through paracrine FGF/TBX3 signaling. Proc Natl Acad Sci U S A 107: 21737-21742. doi: 10.1073/pnas.1007863107 PMID: 21098263
53. Tse HTK, Weaver WM, Di Carlo D (2012) Increased asymmetric and multi-daughter cell division in mechanically confined microenvironments. PLoS One 7: e38986. doi: 10.1371/journal.pone.0038986 PMID: 22761717
54. Medema JP (2013) Cancer stem cells: The challenges ahead. Nature Cell Biol 15: 338-344. doi: 10.1038/ncb2717 PMID: 23548926
55. Boyd NF, Li Q, Melnichouk O, Huszti E, Martin LJ, Gunasekara A, et al. (2014) Evidence that breast tissue stiffness is associated with risk of breast cancer. PLoS One 9: e100937. doi: 10.1371/journal.pone.0100937 PMID: 25010427
56. Tilghman RW, Cowan CR, Mih JD, Koryakina Y, Gioeli D, Slack-Davis JK, et al. (2010) Matrix rigidity regulates cancer cell growth and cellular phenotype. PLoS One 5: e12905. doi: 10.1371/journal.pone.0012905 PMID: 20886123
57. Biddle A, Mackenzie IC (2012) Cancer stem cells and emt in carcinoma. Cancer Metastasis Rev 31: 285-293.
58. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715. doi: 10.1016/j.cell.2008.03.027 PMID: 18485877
59. Zeisberg M, Neilson EG (2009) Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 119: 1429. doi: 10.1172/JCI36183 PMID: 19487819
60. Lamouille S, Xu J, Derynck R (2014) Molecular mechanisms of epithelial-mesenchymal transition. Nature Rev Mol Cell Biol 15: 178-196.
61. Kalluri R, Weinberg RA (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428. doi: 10.1172/JCI39104 PMID: 19487818
62. Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, et al. (2011) The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147: 759-772. doi: 10.1016/j.cell.2011.09.048 PMID: 22078877
63. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, et al. (2011) Role of YAP/TAZ in mechanotransduction. Nature 474: 179-U212. doi: 10.1038/nature10137 PMID: 21654799
64. Staubach S, Hanisch FG (2011) Lipid rafts: Signaling and sorting platforms of cells and their roles in cancer. Expert Rev Proteomics 8: 263-277. doi: 10.1586/epr.11.2 PMID: 21501018
65. Ferraro JT, Daneshmand M, Bizios R, Rizzo V (2004) Depletion of plasma membrane cholesterol dampens hydrostatic pressure and shear stress-induced mechanotransduction pathways in osteoblast cultures. Am J Physiol Cell Physiol 286: C831-C839. PMID: 14644772
66. Ye J, Wu D, Wu P, Chen ZG, Huang J (2014) The cancer stem cell niche: Cross talk between cancer stem cells and their microenvironment. Tumor Biol 35: 3945-3951