3D Electrospun scaffolds promote a cytotrophic phenotype of cultured primary astrocytes

Journal of Neurochemistry

Volumn 130, Issue 2, 2014, Pages 215-226

  Lau, Chew L ^a   Kovacevic, Michelle ^a   Tingleff, Tine S ^a,b   Forsythe, John S ^c   Cate, Holly S ^a   Merlo, Daniel ^a   Cederfur, Cecilia ^a   Maclean, Francesca L ^d   Parish, Clare L ^a   Horne, Malcolm K ^a   Nisbet, David R ^a,c   Beart, Philip M ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c MONASH UNIVERSITY   (Australia)

^d AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

astrocyte; astrogliosis; bioengineering; cell culture; cytotrophic phenotype; gene expression

Indexed keywords

3D ELECTROSPUN SCAFFOLD; BRAIN DERIVED NEUROTROPHIC FACTOR; EXCITATORY AMINO ACID TRANSPORTER 2; F ACTIN; G ACTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MOLECULAR SCAFFOLD; POLYCAPROLACTONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; ASTROCYTE CULTURE; BIOENGINEERING; CELL MIGRATION; CELL PROLIFERATION; CELL STRESS; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOCHEMISTRY; CYTOSKELETON; ELECTROSPINNING; GENE CONTROL; MOUSE; NERVE CELL; NERVE CELL GROWTH; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRESS FIBER; TISSUE REPAIR; UPREGULATION;

MURINAE;

ASTROCYTE; ASTROGLIOSIS; BIOENGINEERING; CELL CULTURE; CYTOTROPHIC PHENOTYPE; GENE EXPRESSION;

ANIMALS; ASTROCYTES; BLOTTING, WESTERN; CELL DIVISION; CELL SURVIVAL; CYTOLOGICAL TECHNIQUES; CYTOSKELETON; FOREIGN-BODY REACTION; GENE EXPRESSION; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; NERVE TISSUE PROTEINS; POLYESTERS; PRIMARY CELL CULTURE; REAL-TIME POLYMERASE CHAIN REACTION; RNA;

EID: 84904071598     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12702     Document Type: Article

References (50)

1. Abe K., and, Misawa M., (2003) Astrocyte stellation induced by Rho kinase inhibitors in culture. Brain Res. Dev. Brain Res. 143, 99-104. (Pubitemid 36588686)
2. Apricò K., Beart P. M., Crawford D., and, O'Shea R. D., (2004) Binding and transport of [3H](2S,4R)- 4-methylglutamate, a new ligand for glutamate transporters, demonstrate labeling of EAAT1 in cultured murine astrocytes. J. Neurosci. Res. 75, 751-759. (Pubitemid 38296088)
3. Beart P. M., and, O'Shea R. D., (2007) Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br. J. Pharmacol. 150, 5-17. (Pubitemid 46094664)
4. Beart P. M., Kovacevic M., Lau C. L., Horne M. K., Forsythe J. S., and, Nisbet D. R., (2012) Astrocytes maintained on 3D nanofibrous scaffolds exhibit healthy morphologies appropriate for regenerative neurobiology, in Transactions of the American Society for Neurochemistry for 43rd ASN Annual Meeting; March 3-7 (, Rasband M., ed.), p. 101. American Society for Neurochemistry, Baltimore.
5. Binder M. D., Cate H. S., Prieto A. L., Kemper D., Butzkueven H., Gresle M. M., Cipriani T., Jokubaitis V. G., Carmeliet P., and, Kilpatrick T. J., (2008) Gas6 deficiency increases oligodendrocyte loss and microglial activation in response to cuprizone-induced demyelination. J. Neurosci. 28, 5195-5206.
6. Cao H., Marcy G., Goh E. L., Wang F., Wang J., and, Chew S. Y., (2012) The effects of nanofiber topography on astrocyte behavior and gene silencing efficiency. Macromol. Biosci. 12, 666-674.
7. Cimarosti H., Jones N. M., O'Shea R. D., Pow D. V., Salbego C., and, Beart P. M., (2005) Hypoxic preconditioning in neonatal rat brain involves regulation of excitatory amino acid transporter 2 and estrogen receptor alpha. Neurosci. Lett. 385, 52-57. (Pubitemid 40909981)
8. East E., de Oliveira D. B., Golding J. P., and, Phillips J. B., (2010) Alignment of astrocytes increases neuronal growth in three-dimensional collagen gels and is maintained following plastic compression to form a spinal cord repair conduit. Tissue Eng. Part A 16, 3173-3184.
9. Etienne-Manneville S., and, Hall A., (2002) Rho GTPases in cell biology. Nature 420, 629-635. (Pubitemid 36764489)
10. Gerardo-Nava J., Führmann T., Klinkhammer K., Seiler N., Mey J., Klee D., Möller M., Dalton P. D., and, Brook G. A., (2009) Human neural cell interactions with orientated electrospun nanofibers in vitro. Nanomedicine (Lond) 4, 11-30.
11. Goldman J. E., and, Abramson B., (1990) Cyclic AMP-induced shape changes of astrocytes are accompanied by rapid depolymerization of actin. Brain Res. 528, 189-196. (Pubitemid 20318195)
12. Gourley S. L., Espitia J. W., Sanacora G., and, Taylor J. R., (2012) Antidepressant-like properties of oral riluzole and utility of incentive disengagement models of depression in mice. Psychopharmacology 219, 805-814.
13. Hall A., (1998) Rho GTPases and the actin cytoskeleton. Science 279, 509-514. (Pubitemid 28067271)
14. Horne M. K., Nisbet D. R., Forsythe J. S., and, Parish C. L., (2010) Three-dimensional nanofibrous scaffolds incorporating immobilized BDNF promote proliferation and differentiation of cortical neural stem cells. Stem Cells Dev. 19, 843-852.
15. Kim S. H., Shin C., Min S. K., Jung S. M., and, Shin H. S., (2012) In vitro evaluation of the effects of electrospun PCL nanofiber mats containing the microalgae Spirulina (Arthrospira) extract on primary astrocytes. Colloids Surf. B Biointerfaces 90, 113-118.
16. Kimelberg H. K., (2004) The problem of astrocyte identity. Neurochem. Int. 45, 191-202. (Pubitemid 38625613)
17. Lau C. L., Beart P. M., and, O'Shea R. D., (2010) Transportable and non-transportable inhibitors of L-glutamate uptake produce astrocytic stellation and increase EAAT2 cell surface expression. Neurochem. Res. 35, 735-742.
18. Lau C. L., O'Shea R. D., Broberg B. V., Bischof L., and, Beart P. M., (2011) The Rho kinase inhibitor Fasudil up-regulates astrocytic glutamate transport subsequent to actin remodelling in murine cultured astrocytes. Br. J. Pharmacol. 163, 533-545.
19. Lau C. L., Perreau V. M., Chen M. J., Cate H. S., Merlo D., Cheung N. S., O'Shea R. D., and, Beart P. M., (2012) Transcriptomic profiling of astrocytes treated with the Rho kinase inhibitor fasudil reveals cytoskeletal and pro-survival responses. J. Cell. Physiol. 227, 1199-1211.
20. Le Clainche C., and, Carlier M. F., (2008) Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol. Rev. 88, 489-513. (Pubitemid 351520086)
21. Maragakis N. J., and, Rothstein J. D., (2006) Mechanisms of disease: astrocytes in neurodegenerative disease. Nat. Clin. Pract. Neurol. 2, 679-689. (Pubitemid 44782682)
22. Martz E., and, Steinberg M. S., (1972) The role of cell-cell contact in "contact" inhibition of cell division: a review and new evidence. J. Cell. Physiol. 79, 189-210.
23. Mattila P. K., and, Lappalainen P., (2008) Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-454. (Pubitemid 351733400)
24. McMillian M. K., Thai L., Hong K. S., O'Callaghan J. P., and, Pennypacker K. R., (1994) Brain injury in a dish: a model for reactive gliosis. Trends Neurosci. 17, 138-142. (Pubitemid 24088182)
25. Meng F., Hlady V., and, Tresco P. A., (2012) Inducing alignment in astrocyte tissue constructs by surface ligands patterned on biomaterials. Biomaterials 33, 1323-1335.
26. Middeldorp J., and, Hol E. M., (2011) GFAP in health and disease. Prog. Neurobiol. 93, 421-443.
27. Mueller B. K., Mueller R., and, Schoemaker H., (2009) Stimulating neuroregeneration as a therapeutic drug approach for traumatic brain injury. Br. J. Pharmacol. 157, 675-685.
28. Nisbet D. R., Yu L. M., Zahir T., Forsythe J. S., and, Shoichet M. S., (2008) Characterization of neural stem cells on electrospun poly(epsilon- caprolactone) submicron scaffolds: evaluating their potential in neural tissue engineering. J. Biomater. Sci. Polym. Ed. 19, 623-634. (Pubitemid 351535785)
29. Nisbet D. R., Rodda A. E., Horne M. K., Forsythe J. S., and, Finkelstein D. I., (2009) Neurite infiltration and cellular response to electrospun polycaprolactone scaffolds implanted into the brain. Biomaterials 30, 4573-4580.
30. O'Neill C., Jordan P., and, Ireland G., (1986) Evidence for two distinct mechanisms of anchorage stimulation in freshly explanted and 3T3 Swiss mouse fibroblasts. Cell 44, 489-496. (Pubitemid 16043339)
31. O'Shea R. D., Lau C. L., Farso M. C., et al,. (2006) Effects of lipopolysaccharide on glial phenotype and activity of glutamate transporters: evidence for delayed up-regulation and redistribution of GLT-1. Neurochem. Int. 48, 604-610.
32. Owen S. C., and, Shoichet M. S., (2010) Design of three-dimensional biomimetic scaffolds. J. Biomed. Mater Res. A 94, 1321-1331.
33. Panickar K. S., and, Norenberg M. D., (2005) Astrocytes in cerebral ischemic injury: morphological and general considerations. Glia 50, 287-298. (Pubitemid 40780835)
34. Parish C. L., Finkelstein D. I., Tripanichkul W., Satoskar A. R., Drago J., and, Horne M. K., (2002) The role of interleukin-1, interleukin-6, and glia in inducing growth of neuronal terminal arbors in mice. J. Neurosci. 22, 8034-8041. (Pubitemid 35379109)
35. Parpura V., Heneka M. T., Montana V., et al,. (2012) Glial cells in (patho)physiology. J. Neurochem. 121, 4-27.
36. Provenzano P. P., and, Keely P. J., (2011) Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J. Cell Sci. 124, 1195-1205.
37. Puschmann T. B., Zandén C., De Pablo Y., Kirchhoff F., Pekna M., Liu J., and, Pekny M., (2013) Bioactive 3D cell culture system minimizes cellular stress and maintains the in vivo-like morphological complexity of astroglial cells. Glia 61, 432-440.
38. Ridet J. L., Malhotra S. K., Privat A., and, Gage F. H., (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20, 570-577. (Pubitemid 27508969)
39. Schnell E., Klinkhammer K., Balzer S., Brook G., Klee D., Dalton P., and, Mey, (2007) J. Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-epsilon-caprolactone and a collagen/poly-epsilon- caprolactone blend. Biomaterials 28, 3012-3025. (Pubitemid 46560871)
40. Sheean R. K., Lau C. L., Shin Y. S., O'Shea R. D., and, Beart P. M., (2013) Links between l-glutamate transporters, Na(+)/K(+)-ATPase and cytoskeleton in astrocytes: evidence following inhibition with rottlerin. Neuroscience 254, 335-346.
41. Singhvi R., Kumar A., Lopez G. P., Stephanopoulos G. N., Wang D. I., Whitesides G. M., and, Ingber D. E., (1994) Engineering cell shape and function. Science 264, 696-698. (Pubitemid 24185878)
42. Sofroniew M. V., (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32, 638-647.
43. Sofroniew M. V., and, Vinters H. V., (2010) Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35.
44. Sorensen A., Alekseeva T., Katechia K., Robertson M., Riehle M. O., and, Barnett S. C., (2007) Long-term neurite orientation on astrocyte monolayers aligned by microtopography. Biomaterials 28, 5498-5508. (Pubitemid 47603198)
45. Stevens M. M., Mayer M., Anderson D. G., Weibel D. B., Whitesides G. M., and, Langer R., (2005) Direct patterning of mammalian cells onto porous tissue engineering substrates using agarose stamps. Biomaterials 26, 7636-7641. (Pubitemid 41187563)
46. Teo W. E., He W., and, Ramakrishna S., (2006) Electrospun scaffold tailored for tissue-specific extracellular matrix. Biotechnol. J. 9, 918-929.
47. Wang X. L., Yu T., Zhang J. S., Yan Q. C., and, Luo Y. H., (2009) Fibronectin and focal adhesion kinase small interfering RNA modulate rat retinal Müller cells adhesion and migration. Cell. Mol. Neurobiol. 29, 549-556.
48. Xu S., Han J. C., Morales A., Menzie C. M., Williams K., and, Fan Y. S., (2008) Characterization of 11p14-p12 deletion in WAGR syndrome by array CGH for identifying genes contributing to mental retardation and autism. Cytogenet. Genome Res. 122, 181-187.
49. Zagami C. J., Beart P. M., Wallis N., Nagley P., and, O'Shea R. D., (2009) Oxidative and excitotoxic insults exert differential effects on spinal motoneurons and astrocytic glutamate transporters: Implications for the role of astrogliosis in amyotrophic lateral sclerosis. Glia 57, 119-135.
50. Zuidema J. M., Hyzinski-García M. C., Van Vlasselaer K., Zaccor N. W., Plopper G. E., Mongin A. A., and, Gilbert R. J., (2014) Enhanced GLT-1 mediated glutamate uptake and migration of primary astrocytes directed by fibronectin-coated electrospun poly-l-lactic acid fibers. Biomaterials 35, 1439-1449.