Electrospun nanofibers as a bioadhesive platform for capturing adherent leukemia cells
Xue Cao
Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, Singapore
Search for more papers by this authorKenneth Kwek
Department of Maternal Fetal Medicine, KK Women's and Children's Hospital, Singapore
Search for more papers by this authorJerry K. Y. Chan
Department of Reproductive Medicine, KK Women's and Children's Hospital, Singapore
Cancer and Stem Cell Biology Program, Duke-NUS Graduate Medical School, Singapore
Experimental Fetal Medicine Group, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
Search for more papers by this authorCasey K. H. Chan
Department of Bioengineering, Faculty of Engineering, National University of Singapore, Singapore
Department of Orthopaedic Surgery, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
Search for more papers by this authorCorresponding Author
Mayasari Lim
Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, Singapore
Correspondence to: M. Lim; e-mail: [email protected]Search for more papers by this authorXue Cao
Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, Singapore
Search for more papers by this authorKenneth Kwek
Department of Maternal Fetal Medicine, KK Women's and Children's Hospital, Singapore
Search for more papers by this authorJerry K. Y. Chan
Department of Reproductive Medicine, KK Women's and Children's Hospital, Singapore
Cancer and Stem Cell Biology Program, Duke-NUS Graduate Medical School, Singapore
Experimental Fetal Medicine Group, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
Search for more papers by this authorCasey K. H. Chan
Department of Bioengineering, Faculty of Engineering, National University of Singapore, Singapore
Department of Orthopaedic Surgery, Yong Loo Lin School of Medicine, National University of Singapore, Singapore
Search for more papers by this authorCorresponding Author
Mayasari Lim
Division of Bioengineering, School of Chemical and Biomedical Engineering, Nanyang Technological University, Singapore
Correspondence to: M. Lim; e-mail: [email protected]Search for more papers by this authorAbstract
This study investigated the adhesive behaviors of normal and abnormal hematopoietic cells on nanotopographical materials. Previously, electrospun nanofiber scaffolds (NFSs) were used to capture and expand hematopoietic stem cells in vitro; here, we demonstrate that NFS could also serve as a useful bioadhesive platform for capturing functionally adherent leukemia cells. Collagen-blended poly(d,l-lactide-co-glycolide) NFS enabled more rapid and efficient capture of K562 leukemia cells than tissue culture polystyrene surfaces with up to 70% improved adhesion and shorter time. Cellular extensions, stronger adhesion, and enhanced cell–cell interactions were observed in K562 cells captured on NFS. While NFS promoted hematopoietic progenitor cell proliferation, it inhibited leukemia cell proliferation and affected cell cycle status by shifting more cells toward the G0/G1 phase. The expression of α-integrins was equally high in both captured and uncaptured leukemia cell populations demonstrating no relation to its adhesive nature. Hematopoietic morphological signatures of NFS captured cells presented no impact on cell differentiation. We conclude that electrospun NFS serves as an excellent platform not only for capturing functionally adherent leukemia cells but also for studying the impact of niche-like structure in the nanoscale. © 2013 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 102A: 523–531, 2014.
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REFERENCES
- 1Salesse S, Verfaillie CM. Mechanisms underlying abnormal trafficking and expansion of malignant progenitors in CML: BCR/ABL-induced defects in integrin function in CML. Oncogene 2002; 21: 8605–8611.
- 2Verfaillie C, Hurley R, Bhatia R, McCarthy JB. Role of bone marrow matrix in normal and abnormal hematopoiesis. Crit Rev Oncol Hematol 1994; 16: 201–224.
- 3Tsai RYL. A molecular view of stem cell and cancer cell self-renewal. Int J Biochem Cell Biol 2003; 36: 684–694.
- 4Ema H, Nakauchi H. Self-renewal and lineage restriction of hematopoietic stem cells. Curr Opin Genet Dev 2003; 13: 508–512.
- 5Stein MI, Zhu J, Emerson SG. Molecular pathways regulating the self-renewal of hematopoietic stem cells. Exp Hematol 2004; 32: 1129–1136.
- 6Thomas X, Anglaret B, Bailly M, Maritaz O, Magaud J-P, Archimbaud E. Differential adhesiveness between blood and marrow leukemic cells having similar pattern of VLA adhesion molecule expression. Leuk Res 1998; 22: 953–960.
- 7Bearpark AD, Gordon MY. Adhesive properties distinguish sub-populations of haemopoietic stem cells with different spleen colony-forming and marrow repopulating capacities. Bone Marrow Transplant 1989; 4: 625–628.
- 8Verfaillie CM, McCarthy JB, McGlave PB. Mechanisms underlying abnormal trafficking of malignant progenitors in chronic myelogenous leukemia. Decreased adhesion to stroma and fibronectin but increased adhesion to the basement membrane components laminin and collagen type IV. J Clin Invest 1992; 90: 1232–1241.
- 9Ma PX, Zhang R. Synthetic nano-scale fibrous extracellular matrix. J Biomed Mater Res 1999; 46: 60–72.
10.1002/(SICI)1097-4636(199907)46:1<60::AID-JBM7>3.0.CO;2-H CAS PubMed Web of Science® Google Scholar
- 10Xu C, Inai R, Kotaki M, Ramakrishna S. Electrospun nanofiber fabrication as synthetic extracellular matrix and its potential for vascular tissue engineering. Tissue Eng 2004; 10: 1160–1168.
- 11Beachley V, Wen X. Polymer nanofibrous structures: Fabrication, biofunctionalization, and cell interactions. Prog Polym Sci 2010; 35: 868–892.
- 12Chua K-N, Chai C, Lee P-C, Ramakrishna S, Leong KW, Mao H-Q. Functional nanofiber scaffolds with different spacers modulate adhesion and expansion of cryopreserved umbilical cord blood hematopoietic stem/progenitor cells. Exp Hematol 2007; 35: 771–781.
- 13Lee CH, Shin HJ, Cho IH, Kang Y-M, Kim IA, Park K-D, Shin J-W. Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast. Biomaterials 2005; 26: 1261–1270.
- 14Chua K-N, Chai C, Lee P-C, Tang Y-N, Ramakrishna S, Leong KW, Mao H-Q. Surface-animated electrospun nanofibers enhance adhesion and expansion of human umbilical cord blood hematopoietic stem/progenitor cells. Biomaterials 2006; 27: 6043–6051.
- 15Vasita R, Katti DS. Nanofibers and their applications in tissue engineering. Int J Nanomed 2006; 1: 15–30.
- 16Koenigsmann M, Griffin J, DiCarlo J, Cannistra S. Myeloid and erythroid progenitor cells from normal bone marrow adhere to collagen type I. Blood 1992; 79: 657–665.
- 17Ma K, Chan CK, Liao S, Hwang WYK, Feng Q, Ramakrishna S. Electrospun nanofiber scaffolds for rapid and rich capture of bone marrow-derived hematopoietic stem cells. Biomaterials 2008; 29: 2096–2103.
- 18Cipitria A, Skelton A, Dargaville TR, Dalton PD, Hutmacher DW. Design, fabrication and characterization of PCL electrospun scaffolds—A review. J Mater Chem 2011; 21: 9419–9428.
- 19Feng Q, Chai C, Jiang X-S, Leong KW, Mao H-Q. Expansion of engrafting human hematopoietic stem/progenitor cells in three-dimensional scaffolds with surface-immobilized fibronectin. J Biomed Mater Res Part A 2006; 78A: 781–791.
- 20Verfaillie CM. Adhesion receptors as regulators of the hematopoietic process. Blood 1998; 92: 2609–2612.
- 21Rood PML, Gerritsen WR, Kramer D, Ranzijn C, von dem Borne AEGK, van der Schoot CE. Adhesion of hematopoietic progenitor cells to human bone marrow or umbilical vein derived endothelial cell lines: A comparison. Exp Hematol 1999; 27: 1306–1314.
- 22Rood PM, Dercksen MW, Cazemier H, Kerst JM, Von dem Borne AE, Gerritsen WR, van der Schoot CE. E-selectin and very late activation antigen-4 mediate adhesion of hematopoietic progenitor cells to bone marrow endothelium. Ann Hematol 2000; 79: 477–484.
- 23Craddock CF, Nakamoto B, Elices M, Papayannopoulou T. The role of CS1 moiety of fibronectin in VLA4-mediated haemapoietic progenitor trafficking. Br J Haematol 1997; 97: 15–21.
- 24Giet O, Huygen S, Beguin Y, Gothot A. Cell cycle activation of hematopoietic progenitor cells increases very late antigen-5-mediated adhesion to fibronectin. Exp Hematol 2001; 29: 515–524.
- 25Weinstein R, Riordan M, Wenc K, Kreczko S, Zhou M, Dainiak N. Dual role of fibronectin in hematopoietic differentiation. Blood 1989; 73: 111–116.
- 26Park SH, Kim TG, Kim HC, Yang D-Y, Park TG. Development of dual scale scaffolds via direct polymer melt deposition and electrospinning for applications in tissue regeneration. Acta Biomater 2008; 4: 1198–1207.
- 27Karchin A, Simonovsky FI, Ratner BD, Sanders JE. Melt electrospinning of biodegradable polyurethane scaffolds. Acta Biomater 2011; 7: 3277–3284.
- 28Jiang X-S, Chai C, Zhang Y, Zhou R-X, Mao H-Q, Leong KW. Surface immobilization of adhesion peptides on substrate for ex vivo expansion of cryopreserved umbilical cord blood CD34+ cells. Biomaterials 2006; 27: 2723–2732.
- 29Yamaguchi M, Hirayama F, Kanai M, Sato N, Fukazawa K, Yamashita K, Sawada K-i, Koike T, Kuwabara M, Ikeda H, Ikebuchi K. Serum-free coculture system for ex vivo expansion of human cord blood primitive progenitors and SCID mouse-reconstituting cells using human bone marrow primary stromal cells. Exp Hematol 2001; 29: 174–182.
- 30Silva CLd, Gonçalves R, Crapnell KB, Cabral J, Zanjani ED, Almeida-Porada G. A human stromal-based serum-free culture system supports the ex vivo expansion/maintenance of bone marrow and cord blood hematopoietic stem/progenitor cells. Exp Hematol 2005; 33: 828–835.
- 31Kobune M, Kawano Y, Takahashi S, Takada K, Murase K, Iyama S, Sato T, Takimoto R, Niitsu Y, Kato J. Interaction with human stromal cells enhances CXCR4 expression and engraftment of cord blood Lin(–)CD34(–) cells. Exp Hematol 2008; 36: 1121–1131.
- 32Lundell B, McCarthy J, Kovach N, Verfaillie C. Activation-dependent alpha5beta1 integrin-mediated adhesion to fibronectin decreases proliferation of chronic myelogenous leukemia progenitors and K562 cells. Blood 1996; 87: 2450–2458.
- 33van der Kuip H, Goetz AW, Miething C, Duyster J, Aulitzky WE. Adhesion to fibronectin selectively protects Bcr-Abl+cells from DNA damage‚ induced apoptosis. Blood 2001; 98: 1532–1541.
- 34Bhatia R, Williams AD, Munthe HA. Contact with fibronectin enhances preservation of normal but not chronic myelogenous leukemia primitive hematopoietic progenitors. Exp Hematol 2002; 30: 324–332.
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