Combined Flow Cytometric Analysis of Surface and Intracellular Antigens Reveals Surface Molecule Markers of Human Neuropoiesis

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Turaç, Gizem ^a,b   Hindley, Christopher J ^a   Thomas, Ria ^a   Davis, Jason A ^a   Deleidi, Michela ^c   Gasser, Thomas ^c   Karaöz, Erdal ^b   Pruszak, Jan ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b KOCAELI UNIVERSITY   (Turkey)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; BIOLOGICAL MARKER; CD200 ANTIGEN; CELL ANTIGEN; DOUBLECORTIN; MEMBRANE ANTIGEN; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; PROTEIN TUJ1; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL POPULATION; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROBLASTOMA CELL; PLURIPOTENT STEM CELL;

ANTIGENS, CD; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; CELL MEMBRANE; CELL SEPARATION; FLOW CYTOMETRY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INTRACELLULAR SPACE; NEURONS; REPRODUCIBILITY OF RESULTS;

MAMMALIA;

EID: 84879486703     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068519     Document Type: Article

References (43)

1. Rieseberg M, Kasper C, Reardon KF, Scheper T, (2001) Flow cytometry in biotechnology. Appl Microbiol Biotechnol 56: 350-360. doi:10.1007/s002530100673. PubMed: 11549001.
2. Jaye DL, Bray RA, Gebel HM, Harris WA, Waller EK, (2012) Translational applications of flow cytometry in clinical practice. J Immunol 188: 4715-4719. doi:10.4049/jimmunol.1290017. PubMed: 22556132.
3. Seita J, Weissman IL, (2010) Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip. Rev Syst Biol Med 2: 640-653.
4. Diogo MM, da Silva CL, Cabral JM, (2012) Separation technologies for stem cell bioprocessing. Biotechnol Bioeng 109: 2699-2709. doi:10.1002/bit.24706. PubMed: 22887094.
5. Israel MA, Goldstein LS, (2011) Capturing Alzheimer's disease genomes with induced pluripotent stem cells: prospects and challenges. Genome Med 3: 49. doi:10.1186/gm265. PubMed: 21867573.
6. Israel MA, Yuan SH, Bardy C, Reyna SM, Mu Y, et al. (2012) Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482: 216-220. PubMed: 22278060.
7. Yuan SH, Martin J, Elia J, Flippin J, Paramban et al,. (2011) Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells. PLOS ONE 6: e17540. doi:10.1371/journal.pone.0017540. PubMed: 21407814.
8. Schriebl K, Satianegara G, Hwang A, Tan HL, Fong WJ, et al. (2012) Selective removal of undifferentiated human embryonic stem cells using magnetic activated cell sorting followed by a cytotoxic antibody. Tissue Eng Part A 18: 899-909. doi:10.1089/ten.tea.2011.0311. PubMed: 22092252.
9. Sánchez-Pernaute R, Studer L, Ferrari D, Perrier A, Lee H, et al. (2005) Long-term survival of dopamine neurons derived from parthenogenetic primate embryonic stem cells (cyno-1) after transplantation. Stem Cells 23: 914-922. doi:10.1634/stemcells.2004-0172. PubMed: 15941857.
10. Schuldiner M, Itskovitz-Eldor J, Benvenisty N, (2003) Selective ablation of human embryonic stem cells expressing a "suicide" gene. Stem Cells 21: 257-265. doi:10.1634/stemcells.21-3-257. PubMed: 12743320.
11. Hedlund E, Pruszak J, Lardaro T, Ludwig W, Viñuela A, et al. (2008) Embryonic stem cell-derived Pitx3-enhanced green fluorescent protein midbrain dopamine neurons survive enrichment by fluorescence-activated cell sorting and function in an animal model of Parkinson's disease. Stem Cells 26: 1526-1536. doi:10.1634/stemcells.2007-0996. PubMed: 18388307.
12. Pruszak J, Ludwig W, Blak A, Alavian K, Isacson O, (2009) CD15, CD24, and CD29 define a surface biomarker code for neural lineage differentiation of stem cells. Stem Cells 27: 2928-2940. PubMed: 19725119.
13. Pruszak J, Sonntag KC, Aung MH, Sanchez-Pernaute R, Isacson O, (2007) Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 25: 2257-2268. doi:10.1634/stemcells.2006-0744. PubMed: 17588935.
14. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, et al. (2005) Direct isolation of satellite cells for skeletal muscle regeneration. Science 309: 2064-2067. doi:10.1126/science.1114758. PubMed: 16141372.
15. Dubois NC, Craft AM, Sharma P, Elliott DA, Stanley EG, et al. (2011) SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat Biotechnol 29: 1011-1018. doi:10.1038/nbt.2005. PubMed: 22020386.
16. Uosaki H, Fukushima H, Takeuchi A, Matsuoka S, Nakatsuji N, et al. (2011) Efficient and scalable purification of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression. PLOS ONE 6: e23657. doi:10.1371/journal.pone.0023657. PubMed: 21876760.
17. Hong S, Hwang DY, Yoon S, Isacson O, Ramezani A, et al. (2007) Functional analysis of various promoters in lentiviral vectors at different stages of in vitro differentiation of mouse embryonic stem cells. Mol Ther 15: 1630-1639. doi:10.1038/sj.mt.6300251. PubMed: 17609656.
18. Sergent-Tanguy S, Chagneau C, Neveu I, Naveilhan P, (2003) Fluorescent activated cell sorting (FACS): a rapid and reliable method to estimate the number of neurons in a mixed population. J Neurosci Methods 129: 73-79. doi:10.1016/S0165-0270(03)00210-3. PubMed: 12951234.
19. Krichevsky AM, Sonntag KC, Isacson O, Kosik KS, (2006) Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24: 857-864. doi:10.1634/stemcells.2005-0441. PubMed: 16357340.
20. Elghetany MT, Davis BH, (2005) Impact of preanalytical variables on granulocytic surface antigen expression: a review. Cytometry B Clin Cytom 65: 1-5. PubMed: 15800882.
21. Kappelmayer J, Gratama JW, Karászi E, Menéndez P, Ciudad J, et al. (2000) Flow cytometric detection of intracellular myeloperoxidase, CD3 and CD79a. Interaction between monoclonal antibody clones, fluorochromes and sample preparation protocols. J Immunol Methods 242: 53-65. doi:10.1016/S0022-1759(00)00220-9. PubMed: 10986389.
22. Deleidi M, Hargus G, Hallett P, Osborn T, Isacson O, (2011) Development of histocompatible primate-induced pluripotent stem cells for neural transplantation. Stem Cells 29: 1052-1063. doi:10.1002/stem.662. PubMed: 21608081.
23. Kriks S, Shim JW, Piao J, Ganat YM, Wakeman DR, et al. (2011) Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480: 547-551. PubMed: 22056989.
24. Jouhilahti EM, Peltonen S, Peltonen J, (2008) Class III beta-tubulin is a component of the mitotic spindle in multiple cell types. J Histochem Cytochem 56: 1113-1119. doi:10.1369/jhc.2008.952002. PubMed: 18796406.
25. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Südhof TC, et al. (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463: 1035-1041. doi:10.1038/nature08797. PubMed: 20107439.
26. Meng F, Chen S, Miao Q, Zhou K, Lao Q, et al. (2012) Induction of fibroblasts to neurons through adenoviral gene delivery. Cell Res 22: 436-440. doi:10.1038/cr.2011.185. PubMed: 22105483.
27. Humphrey RK, Bucay N, Beattie GM, Lopez A, Messam CA, et al. (2003) Characterization and isolation of promoter-defined nestin-positive cells from the human fetal pancreas. Diabetes 52: 2519-2525. doi:10.2337/diabetes.52.10.2519. PubMed: 14514635.
28. Constantinescu R, Constantinescu AT, Reichmann H, Janetzky B, (2007) Neuronal differentiation and long-term culture of the human neuroblastoma line SH-SY5Y. J Neural Transm Suppl: pp. 17-28. PubMed: 17982873.
29. Zhao F, Wu T, Lau A, Jiang T, Huang Z, et al. (2009) Nrf2 promotes neuronal cell differentiation. Free Radic Biol Med 47: 867-879. doi:10.1016/j.freeradbiomed.2009.06.029. PubMed: 19573594.
30. Hall PE, Lathia JD, Miller NG, Caldwell MA, Ffrench-Constant C, (2006) Integrins are markers of human neural stem cells. Stem Cells 24: 2078-2084. doi:10.1634/stemcells.2005-0595. PubMed: 16690778.
31. Adler J, Parmryd I, (2010) Quantifying colocalization by correlation: the Pearson correlation coefficient is superior to the Mander's overlap coefficient. Cytometry A 77: 733-742. PubMed: 20653013.
32. Sonntag KC, Pruszak J, Yoshizaki T, van Arensbergen J, Sanchez-Pernaute R, et al. (2007) Enhanced yield of neuroepithelial precursors and midbrain-like dopaminergic neurons from human embryonic stem cells using the bone morphogenic protein antagonist noggin. Stem Cells 25: 411-418. doi:10.1634/stemcells.2006-0380. PubMed: 17038668.
33. Zelnickova P, Faldyna M, Stepanova H, Ondracek J, Kovaru F, (2007) Intracellular cytokine detection by flow cytometry in pigs: fixation, permeabilization and cell surface staining. J Immunol Methods 327: 18-29. doi:10.1016/j.jim.2007.07.006. PubMed: 17720184.
34. Gerner W, Käser T, Pintaric M, Groiss S, Saalmüller A, (2008) Detection of intracellular antigens in porcine PBMC by flow cytometry: A comparison of fixation and permeabilisation reagents. Vet Immunol Immunopathol 121: 251-259. doi:10.1016/j.vetimm.2007.09.019. PubMed: 18243933.
35. Pollice AA, McCoy JP Jr., Shackney SE, Smith CA, Agarwal J, et al. (1992) Sequential paraformaldehyde and methanol fixation for simultaneous flow cytometric analysis of DNA, cell surface proteins, and intracellular proteins. Cytometry 13: 432-444. doi:10.1002/cyto.990130414. PubMed: 1382010.
36. Hulspas R, O'Gorman MR, Wood BL, Gratama JW, Sutherland DR, (2009) Considerations for the control of background fluorescence in clinical flow cytometry. Cytometry B Clin Cytom 76: 355-364. PubMed: 19575390.
37. Brunlid G, Pruszak J, Holmes B, Isacson O, Sonntag KC, (2007) Immature and neurally differentiated mouse embryonic stem cells do not express a functional Fas/Fas ligand system. Stem Cells 25: 2551-2558. doi:10.1634/stemcells.2006-0745. PubMed: 17615270.
38. Webb M, Barclay AN, (1984) Localisation of the MRC OX-2 glycoprotein on the surfaces of neurones. J Neurochem 43: 1061-1067. doi:10.1111/j.1471-4159.1984.tb12844.x. PubMed: 6147390.
39. Delorme B, Ringe J, Gallay N, Le Vern Y, Kerboeuf D, et al. (2008) Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells. Blood 111: 2631-2635. doi:10.1182/blood-2007-07-099622. PubMed: 18086871.
40. Yu KR, Yang SR, Jung JW, Kim H, Ko K, et al. (2012) CD49f enhances multipotency and maintains stemness through the direct regulation of OCT4 and SOX2. Stem Cells 30: 876-887. doi:10.1002/stem.1052. PubMed: 22311737.
41. Chitnis T, Imitola J, Wang Y, Elyaman W, Chawla P, et al. (2007) Elevated neuronal expression of CD200 protects Wlds mice from inflammation-mediated neurodegeneration. Am J Pathol 170: 1695-1712. doi:10.2353/ajpath.2007.060677. PubMed: 17456775.
42. Walker DG, Dalsing-Hernandez JE, Campbell NA, Lue LF, (2009) Decreased expression of CD200 and CD200 receptor in Alzheimer's disease: a potential mechanism leading to chronic inflammation. Exp Neurol 215: 5-19. doi:10.1016/j.expneurol.2008.09.003. PubMed: 18938162.
43. Preffer F, Dombkowski D, (2009) Advances in complex multiparameter flow cytometry technology: Applications in stem cell research. Cytometry B Clin Cytom. 76: 295-314. PubMed: 19492350.