Effect of CD44 Binding Peptide Conjugated to an Engineered Inert Matrix on Maintenance of Breast Cancer Stem Cells and Tumorsphere Formation

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Yang, Xiaoming ^a,b   Sarvestani, Samaneh K ^a   Moeinzadeh, Seyedsina ^a   He, Xuezhong ^a   Jabbari, Esmaiel ^a  

^a The Department of Mechanical Engineering   (United States)

^b Dorn Research Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA5 INTEGRIN; ARGINYLGLYCYLASPARTIC ACID; BETA3 INTEGRIN; BREAST CANCER RESISTANCE PROTEIN; CD22 ANTIGEN; FIBRONECTIN BINDING PROTEIN; HEPARIN BINDING PROTEIN; HERMES ANTIGEN; INTEGRIN; MACROGOL; NERVE CELL ADHESION MOLECULE; STEM CELL ANTIGEN 1; UVOMORULIN; VASCULOTROPIN; VIMENTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; BREAST CANCER; CANCER STEM CELL; CELL ADHESION; CELL DENSITY; CELL VIABILITY; CONTROLLED STUDY; ENCAPSULATION; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR SPHEROID; TUMOR VOLUME;

ANTIGENS, CD44; BIOLOGICAL MARKERS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; FEMALE; FIBRONECTINS; HUMANS; HYDROGEL; NEOPLASTIC STEM CELLS; OLIGOPEPTIDES; PEPTIDES; PROTEIN BINDING; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 84875079104     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059147     Document Type: Article

References (69)

1. American Cancer Society (2010) Breast cancer facts and figures 2009-2010.
2. Badve S, Nakshatri H, (2012) Breast-cancer stem cells-beyond semantics. Lancet Oncol 13: e43-8.
3. Martin-Belmonte F, Perez-Moreno M, (2011) Epithelial cell polarity, stem cells and cancer. Nat Rev Cancer 12: 23-38.
4. Giatromanolaki A, Sivridis E, Fiska A, Koukourakis MI, (2010) The CD44+/CD24- phenotype relates to 'triple-negative' state and unfavorable prognosis in breast cancer patients. Med Oncol 28: 745-752.
5. Rennstam K, McMichael N, Berglund P, Honeth G, Hegardt C, et al. (2009) Numb protein expression correlates with a basal-like phenotype and cancer stem cell markers in primary breast cancer. Breast Cancer Res Treat 122: 315-24.
6. Cabarcas SM, Mathews LA, Farrar WL, (2011) The cancer stem cell niche-there goes the neighborhood? Int J Cancer 129: 2315-27.
7. Dawson E, Mapili G, Erickson K, Taqvi S, Roy K, (2008) Biomaterials for stem cell differentiation. Adv Drug Deliv Rev 60: 215-28.
8. Masters KS, Shah DN, Walker G, Leinwand LA, Anseth KS, (2004) Designing scaffolds for valvular interstitial cells: cell adhesion and function on naturally derived materials. J Biomed Mater Res A 71: 172-80.
9. 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: 106-10.
10. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, et al. (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-7.
11. Alves CS, Yakovlev S, Medved L, Konstantopoulos K, (2009) Biomolecular characterization of CD44-fibrin(ogen) binding: distinct molecular requirements mediate binding of standard and variant isoforms of CD44 to immobilized fibrin(ogen). J Biol Chem 284: 1177-89.
12. Masuko K, Okazaki S, Satoh M, Tanaka G, Ikeda T, et al. (2012) Anti-tumor effect against human cancer xenografts by a fully human monoclonal antibody to a variant 8-epitope of CD44R1 expressed on cancer stem cells. PLoS One 7: e29728.
13. Majeti R, (2011) Monoclonal antibody therapy directed against human acute myeloid leukemia stem cells. Oncogene 30: 1009-19.
14. Tremmel M, Matzke A, Albrecht I, Laib AM, Olaku V, et al. (2009) A CD44v6 peptide reveals a role of CD44 in VEGFR-2 signaling and angiogenesis. Blood 114: 5236-44.
15. Pulaski BA, Clements VK, Pipeling MR, Ostrand-Rosenberg S, (2000) Immunotherapy with vaccines combining MHC class II/CD80+ tumor cells with interleukin-12 reduces established metastatic disease and stimulates immune effectors and monokine induced by interferon gamma. Cancer Immunol Immunother 49: 34-45.
16. Kruger JA, Kaplan CD, Luo Y, Zhou H, Markowitz D, et al. (2006) Characterization of stem cell-like cancer cells in immune-competent mice. Blood 108: 3906-12.
17. Moeinzadeh S, Barati S, He X, Jabbari E, (2012) Gelation characteristics and osteogenic differentiation of stromal cells in inert hydrolytically degradable micellar polyethylene glycol hydrogels. Biomacromolecules 13: 2073-2086.
18. Hibino S, Shibuya M, Engbring JA, Mochizuki M, Nomizu M, et al. (2004) Identification of an active site on the laminin alpha5 chain globular domain that binds to CD44 and inhibits malignancy. Cancer Res 64: 4810-6.
19. Hurt EM, Chan K, Serrat MA, Thomas SB, Veenstra TD, et al. (2010) Identification of vitronectin as an extrinsic inducer of cancer stem cell differentiation and tumor formation. Stem Cells 28: 390-8.
20. Woods A, McCarthy JB, Furcht LT, Couchman JR, (1993) A synthetic peptide from the COOH-terminal heparin-binding domain of fibronectin promotes focal adhesion formation. Mol Biol Cell 4: 605-13.
21. 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: 12508-16.
22. Yu F, Li J, Chen H, Fu J, Ray 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.
23. Krohn A, Song YH, Muehlberg F, Droll L, Beckmann C, et al. (2009) CXCR4 receptor positive spheroid forming cells are responsible for tumor invasion in vitro. Cancer Letters 280: 65-71.
24. Gupta PB, Onder TT, Jiang GZ, Tao K, Kuperwasser C, et al. (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659.
25. Liu JC, Deng T, Lehal RS, Kim J, Zacksenhaus E, (2007) Identification of tumorsphere- and tumor-initiating cells in HER2/Neu-induced mammary tumors. Cancer Res 67: 8671-81.
26. Fillmore CM, Kuperwasser C, (2008) Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 10: R25.
27. 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.
28. Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H, (2006) Quantitative real-time RT-PCR data analysis: current concepts and the novel "gene expression's CT difference" formula. J Mol Med (Berl) 84: 901-10.
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.
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 A 93: 941-53.
31. You S, Wood PA, Xiong Y, Kobayashi M, Du-Quiton J, et al. (2005) Daily coordination of cancer growth and circadian clock gene expression. Breast Cancer Res Treat 91: 47-60.
32. Shepherd R, Harrap KR, (1982) Modulation of the toxicity and antitumor activity of alkylating drugs by steroids. Br J Cancer 45: 413-420.
33. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate- a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B-Methodol 57: 289-300.
34. 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.
35. Bhat-Nakshatri P, Appaiah H, Ballas C, Pick-Franke P, Goulet R Jr, Badve S, et al. (2010) SLUG/SNAI2 and tumor necrosis factor generate breast cells with CD44+/CD24- phenotype. BMC Cancer 10: 411.
36. Cox RD, Church CD, (2011) Mouse models and the interpretation of human GWAS in type 2 diabetes and obesity. Dis Model Mech 4: 155-164.
37. Wels J, Kaplan RN, Rafii S, Lyden D, (2008) Migratory neighbors and distant invaders: tumor-associated niche cells. Genes Dev 22: 559-574.
38. Del Vecchio CA, Jensen KC, Nitta RT, Shain AH, Giacomini CP, et al. (2012) Epidermal growth factor receptor variant III contributes to cancer stem cell phenotypes in invasive breast carcinoma. Cancer Res 72: 2657-71.
39. Abhold EL, Kiang A, Rahimy E, Kuo SZ, Wang-Rodriguez J, et al. (2012) EGFR kinase promotes acquisition of stem cell-like properties: a potential therapeutic target in head and neck squamous cell carcinoma stem cells. PLoS One 7: e32459.
40. Biddle A, Mackenzie IC (2012) Cancer stem cells and EMT in carcinoma. Cancer Metastasis Rev PMID: 22302111.
41. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, et al. (2012) EMT and dissemination precede pancreatic tumor formation. Cell 148: 349-61.
42. Gravdal K, Halvorsen OJ, Haukaas SA, Akslen LA, (2007) A switch from E-cadherin to N-cadherin expression indicates epithelial to mesenchymal transition and is of strong and independent importance for the progress of prostate cancer. Clin Cancer Res 13: 7003-11.
43. Nieto MA, (2011) The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 27: 347-76.
44. van Roy F, Berx G, (2008) The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci 65: 3756-88.
45. Rathinam R, Alahari SK, (2010) Important role of integrins in the cancer biology. Cancer Metastasis Rev 29: 223-37.
46. Korsching E, Packeisen J, Liedtke C, Hungermann D, Wulfing P, et al. (2005) The origin of vimentin expression in invasive breast cancer: epithelial-mesenchymal transition, myoepithelial histogenesis or histogenesis from progenitor cells with bilinear differentiation potential? J Pathol 206: 451-7.
47. Calvo A, Catena R, Noble MS, Carbott D, Gil-Bazo I, et al. (2008) Identification of VEGF-regulated genes associated with increased lung metastatic potential: functional involvement of tenascin-C in tumor growth and lung metastasis. Oncogene 27: 5373-84.
48. Ercan C, van Diest PJ, Vooijs M, (2011) Mammary development and breast cancer: the role of stem cells. Curr Mol Med 11: 270-85.
49. Butcher DT, Alliston T, Weaver VM, (2009) A tense situation: forcing tumour progression. Nat Rev Cancer 9: 108-22.
50. Jalkanen S, Jalkanen M, (1992) Lymphocyte CD44 binds the COOH-terminal heparin-binding domain of fibronectin. J Cell Biol 116: 817-25.
51. Teriete P, Banerji S, Noble M, Blundell CD, Wright AJ, et al. (2004) Structure of the regulatory hyaluronan binding domain in the inflammatory leukocyte homing receptor CD44. Mol Cell 13: 483-96.
52. Weber GF, Ashkar S, Cantor H, (1997) Interaction between CD44 and osteopontin as a potential basis for metastasis formation. Proc Assoc Am Physicians 109: 1-9.
53. Faassen AE, Schrager JA, Klein DJ, Oegema TR, Couchman JR, et al. (1992) A cell surface chondroitin sulfate proteoglycan, immunologically related to CD44, is involved in type I collagen-mediated melanoma cell motility and invasion. J Cell Biol 116: 521-31.
54. Ponta H, Sherman L, Herrlich PA, (2003) CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4: 33-45.
55. Savani RC, Cao G, Pooler PM, Zaman A, Zhou Z, et al. (2001) Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. J Biol Chem 276: 36770-8.
56. Piotrowicz RS, Damaj BB, Hachicha M, Incardona F, Howell SB, et al. (2011) A6 peptide activates CD44 adhesive activity, induces FAK and MEK phosphorylation, and inhibits the migration and metastasis of CD44-expressing cells. Mol Cancer Ther 10: 2072-82.
57. Giancotti FG, Tarone G, (2003) Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu Rev Cell Dev Biol 19: 173-206.
58. Monferran S, Skuli N, Delmas C, Favre G, Bonnet J, et al. (2008) Alphavbeta3 and alphavbeta5 integrins control glioma cell response to ionising radiation through ILK and RhoB. Int J Cancer 123: 357-64.
59. Rizzo S, Attard G, Hudson DL, (2005) Prostate epithelial stem cells. Cell Prolif 38: 363-74.
60. Galbraith CG, Yamada KM, Sheetz MP, (2002) The relationship between force and focal complex development. J Cell Biol 159: 695-705.
61. Nelson CM, Jean RP, Tan JL, Liu WF, Sniadecki NJ, et al. (2005) Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci U S A 102: 11594-9.
62. Giannone G, Sheetz MP, (2006) Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol 16: 213-23.
63. Yu CH, Law JB, Suryana M, Low HY, Sheetz MP, (2011) Early integrin binding to Arg-Gly-Asp peptide activates actin polymerization and contractile movement that stimulates outward translocation. Proc Natl Acad Sci U S A 108: 20585-90.
64. Akiyama SK, Nagata K, Yamada KM, (1990) Cell surface receptors for extracellular matrix components. Biochim Biophys Acta 1031: 91-110.
65. Owens LV, Xu L, Craven RJ, Dent GA, Weiner TM, et al. (1995) Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res 55: 2752-5.
66. Luo M, Guan JL, (2010) Focal adhesion kinase: a prominent determinant in breast cancer initiation, progression and metastasis. Cancer Lett 289: 127-39.
67. Xu LH, Yang X, Bradham CA, Brenner DA, Baldwin AS, et al. (2000) The focal adhesion kinase suppresses transformation-associated, anchorage-independent apoptosis in human breast cancer cells. Involvement of death receptor-related signaling pathways. J Biol Chem 275: 30597-604.
68. Kang Y, Massague J, (2004) Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118: 277-9.
69. Saha S, Lo PK, Duan X, Chen H, Wang Q, (2012) Breast tumour initiating cell fate is regulated by microenvironmental cues from an extracellular matrix. Integr Biol (Camb) 4: 897-904.