ABC transporters, neural stem cells and neurogenesis - A different perspective

Cell Research

Volumn 16, Issue 11, 2006, Pages 857-871

  Lin, Tingting ^a   Islam, Omedul ^a   Heese, Klaus ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

ABC transporters; ABCB1; ABCG2; Differentiation; Neural stem cells; Stem cell marker

Indexed keywords

ABC TRANSPORTER; ABCB1 PROTEIN, HUMAN; ABCG2 PROTEIN, HUMAN; ORGANIC ANION TRANSPORTER; TUMOR PROTEIN;

ANIMAL; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY; REVIEW; STEM CELL;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION; HUMANS; MODELS, BIOLOGICAL; NEOPLASM PROTEINS; NEURONS; ORGANIC ANION TRANSPORTERS; STEM CELLS;

EID: 33751075186     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/sj.cr.7310107     Document Type: Review

References (181)

1. Priddle H, Jones DR, Burridge PW, Patient R. Hematopoiesis from human embryonic stem cells: overcoming the immune barrier in stem cell therapies. Stem Cells 2006; 24:815-824.
2. Taupin P. Neurogenesis in the adult central nervous system. C R Biol 2006; 329:465-475.
3. Erlandsson A, Morshead CM. Exploiting the properties of adult stem cells for the treatment of disease. Curr Opin Mol Ther 2006; 8:331-337.
4. Chan RJ, Yoder MC. The multiple facets of hematopoietic stem cells. Curr Neurovasc Res 2004; 1:197-206.
5. Bonnet D. Normal and leukaemic stem cells. Br J Haematol 2005; 130:469-479.
6. Wu M, Wei YQ. Development of respiratory stem cells and progenitor cells. Stem Cells Dev 2004; 13:607-613.
7. Challen GA, Little MH. A side order of stem cells: the SP phenotype. Stem Cells 2006; 24:3-12
8. Jackson KA, Majka SM, Wang H, et al. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 2001; 107:1395-1402.
9. Goodell MA, Brose K, Paradis G, et al. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996; 183:1797-1806.
10. Weissman IL. Stem cells: units of development, units of regeneration, and units in evolution. Cell 2000; 100:157-168.
11. Shostak S. (Re)defining stem cells. Bioessays 2006; 28:301-308.
12. Venezia TA, Merchant AA, Ramos CA, et al. Molecular signatures of proliferation and quiescence in hematopoietic stem cells. PLoS Biol 2004; 2:e301.
13. Wilson A, Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 2006; 6:93-106.
14. Rizo A, Vellenga E, de Haan G, Schuringa JJ. Signaling pathways in self-renewing hematopoietic and leukemic stem cells: do all stem cells need a niche? Hum Mol Genet 2006; 15:R210-R219.
15. Scadden DT. The stem-cell niche as an entity of action. Nature 2006; 441:1075-1079.
16. Oliveira AA Jr., Hodges HM. Alzheimer's disease and neural transplantation as prospective cell therapy. Curr Alzheimer Res 2005; 2:79-95.
17. Tanne JH. Activating stem cells may treat Alzheimer's. BMJ 2005; 330:622.
18. Lindvall O, Kokaia Z. Stem cells for the treatment of neurological disorders. Nature 2006; 441:1094-1096.
19. Selkoe DJ, Schenk D. Alzheimer's disease: molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 2003; 43:545-584.
20. Swerdlow RH. Is aging part of Alzheimer's disease, or is Alzheimer's disease part of aging? Neurobiol Aging 2006. Epub ahead of print.
21. Harman D. Alzheimer's disease pathogenesis: role of aging. Ann NY Acad Sci 2006; 1067:454-460.
22. Brazel CY, Rao MS. Aging and neuronal replacement. Ageing Res Rev 2004; 3:465-483.
23. Sailor KA, Ming GL, Song H. Neurogenesis as a potential therapeutic strategy for neurodegenerative diseases. Expert Opin Biol Ther 2006; 6:879-890.
24. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005; 28:223-250.
25. Okano H. Adult neural stem cells and central nervous system repair. Ernst Schering Res Found Workshop 2006; 60:215-228.
26. Tabar V, Panagiotakos G, Greenberg ED, et al. Migration and differentiation of neural precursors derived from human embryonic stem cells in the rat brain. Nat Biotechnol 2005; 23:601-606.
27. Jagasia R, Song H, Gage FH, Lie DC. New regulators in adult neurogenesis and their potential role for repair. Trends Mol Med 2006; 12:400-405.
28. Lennington JB, Yang Z, Conover JC. Neural stem cells and the regulation of adult neurogenesis. Reprod Biol Endocrinol 2003; 1:99.
29. Gage FH. Mammalian neural stem cells. Science 2000; 287:1433-1438.
30. Shih CC, Weng Y, Mamelak A, et al. Identification of a candidate human neurohematopoietic stem-cell population. Blood 2001; 98:2412-2422.
31. Muller FJ, Snyder EY, Loring JF. Gene therapy: can neural stem cells deliver? Nat Rev Neurosci 2006; 7:75-84.
32. Aboody KS, Brown A, Rainov NG, et al. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 2000; 97:12846-12851.
33. Chi L, Ke Y, Luo C, et al. Motor neuron degeneration promotes neural progenitor cell proliferation, migration, and neurogenesis in the spinal cords of amyotrophic lateral sclerosis mice. Stem Cells 2006; 24:34-43.
34. Glass R, Synowitz M, Kronenberg G, et al. Glioblastoma-induced attraction of endogenous neural precursor cells is associated with improved survival. J Neurosci 2005; 25:2637-2646.
35. Brown AB, Yang W, Schmidt NO, et al. Intravascular delivery of neural stem cell lines to target intracranial and extracranial tumors of neural and non-neural origin. Hum Gene Ther 2003; 14:1777-1785.
36. Kelly S, Bliss TM, Shah AK, et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci USA 2004; 101:11839-11844.
37. Fernaud-Espinosa I, Nieto-Sampedro M, Bovolenta P. Differential activation of microglia and astrocytes in aniso- and isomorphic gliotic tissue. Glia 1993; 8:277-291.
38. Wang K, Walz W. Unusual topographical pattern of proximal astrogliosis around a cortical devascularizing lesion. J Neurosci Res 2003; 73:497-506.
39. Hulspas R, Quesenberry PJ. Characterization of neurosphere cell phenotypes by flow cytometry. Cytometry 2000; 40:245-250.
40. Campos LS. Neurospheres: insights into neural stem cell biology. J Neurosci Res 2004; 78:761-769.
41. Reynolds BA, Rietze RL. Neural stem cells and neurospheres - re-evaluating the relationship. Nat Methods 2005; 2:333-336.
42. Engstrom CM, Demers D, Dooner M, et al. A method for clonal analysis of epidermal growth factor-responsive neural progenitors. J Neurosci Methods 2002; 117:111-121.
43. Kanemura Y, Mori H, Kobayashi S, et al. Evaluation of in vitro proliferative activity of human fetal neural stem/progenitor cells using indirect measurements of viable cells based on cellular metabolic activity. J Neurosci Res 2002; 69:869-879.
44. Garcion E, Halilagic A, Faissner A, et al. Generation of an environmental niche for neural stem cell development by the extracellular matrix molecule tenascin C. Development 2004; 131:3423-3432.
45. Nagato M, Heike T, Kato T, et al. Prospective characterization of neural stem cells by flow cytometry analysis using a combination of surface markers. J Neurosci Res 2005; 80:456-466.
46. Doetsch F. The glial identity of neural stem cells. Nat Neurosci 2003; 6:1127-1134.
47. Widera D, Mikenberg I, Kaus A, Kaltschmidt C, Kaltschmidt B. Nuclear Factor-kappaB controls the reaggregation of 3D neurospheres culture in vitro. Eur Cell Mater 2006; 11:76-85.
48. Schafer KH, Hagl CI, Rauch U. Differentiation of neurospheres from the enteric nervous system. Pediatr Surg Int 2003; 19:340-344.
49. Pevny L, Rao MS. The stem-cell menagerie. Trends Neurosci 2003; 26:351-359.
50. Bottai D, Fiocco R, Gelain F, et al. Neural stem cells in the adult nervous system. J Hematother Stem Cell Res 2003; 12:655-670.
51. Conti L, Pollard SM, Gorba T, et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 2005; 3:e283.
52. Klein C, Fishell G. Neural stem cells: progenitors or panacea? Dev Neurosci 2004; 26:82-92.
53. Kaminski WE, Piehler A, Wenzel JJ. ABC A-subfamily transporters: structure, function and disease. Biochim Biophys Acta 2006; 1762:510-524.
54. Latunde-Dada GO, Simpson RJ, McKie AT. Recent advances in mammalian haem transport. Trends Biochem Sci 2006; 31:182-188.
55. Deeley RG, Westlake C, Cole SP. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 2006; 86:849-899.
56. Perez-Tomas R. Multidrug resistance: retrospect and prospects in anti-cancer drug treatment. Curr Med Chem 2006; 13:1859-1876.
57. Balayssac D, Authier N, Cayre A, et al. Does inhibition of P-glycoprotein lead to drug-drug interactions? Toxicol Lett 2005; 156:319-329.
58. Sparreboom A, Danesi R, Ando Y, et al. Pharmacogenomics of ABC transporters and its role in cancer chemotherapy. Drug Resist Update 2003; 6:71-84.
59. Teodori E, Dei S, Martelli C, Scapecchi S, Gualtieri F. The functions and structure of ABC transporters: implications for the design of new inhibitors of Pgp and MRP1 to control multidrug resistance (MDR). Curr Drug Targets 2006; 7:893-909.
60. Locher KP. Structure and mechanism of ABC transporters. Curr Opin Struct Biol 2004; 14:426-431.
61. Cavelier C, Lorenzi I, Rohrer L, von Eckardstein A. Lipid efflux by the ATP-binding cassette transporters ABCA1 and ABCG1. Biochim Biophys Acta 2006; 1761:655-666.
62. Pedersen PL. Transport ATPases: structure, motors, mechanism and medicine: a brief overview. J Bioenerg Biomembr 2005; 37:349-357.
63. Al-Shawi MK, Omote H. The remarkable transport mechanism of P-glycoprotein: a multidrug transporter. J Bioenerg Biomembr 2005; 37:489-496.
64. Frelet A, Klein M. Insight in eukaryotic ABC transporter function by mutation analysis. FEBS Lett 2006; 580:1064-1084.
65. Choudhuri S, Klaassen CD. Structure, function, expression, genomic organization, and single nucleotide polymorphisms of human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) efflux transporters. Int J Toxicol 2006; 25:231-259.
66. Kusuhara H, Sugiyama Y. ATP-binding cassette, subfamily G (ABCG family). Pflugers Arch 2006. Epub ahead of print.
67. Abbott BL. ABCG2 (BCRP): a cytoprotectant in normal and malignant stem cells. Clin Adv Hematol Oncol 2006;4:63-72.
68. Wakabayashi K, Tamura A, Saito H, Onishi Y, Ishikawa T. Human ABC transporter ABCG2 in xenobiotic protection and redox biology. Drug Metab Rev 2006; 38:371-391.
69. Wada M. Single nucleotide polymorphisms in ABCC2 and ABCB1 genes and their clinical impact in physiology and drug response. Cancer Lett 2006; 234:40-50.
70. Krishnamurthy P, Schuetz JD. Role of ABCG2/BCRP in biology and medicine. Annu Rev Pharmacol Toxicol 2006; 46:381-410.
71. Rocchi E, Khodjakov A, Volk EL, et al. The product of the ABC half-transporter gene ABCG2 (BCRP/MXR/ABCP) is expressed in the plasma membrane. Biochem Biophys Res Commun 2000; 271:42-46.
72. Doyle LA, Yang W, Abruzzo LV, et al. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 1998; 95:15665-15670.
73. Miyake K, Mickley L, Litman T, et al. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res 1999; 59:8-13.
74. Janvilisri T, Shahi S, Venter H, Balakrishnan L, van Veen HW. Arginine-482 is not essential for transport of antibiotics, primary bile acids and unconjugated sterols by the human breast cancer resistance protein (ABCG2). Biochem J 2005; 385:419-426.
75. van de Water FM, Masereeuw R, Russel FG. Function and regulation of multidrug resistance proteins (MRPs) in the renal elimination of organic anions. Drug Metab Rev 2005; 37:443-471.
76. Klein M, Burla B, Martinoia E. The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett 2006; 580:1112-1122.
77. Polgar O, Bates SE. ABC transporters in the balance: is there a role in multidrug resistance? Biochem Soc Trans 2005; 33:241-245.
78. Tian Q, Zhang J, Chan E, Duan W, Zhou S. Multidrug resistance proteins (MRPs) and implications in drug development. Drug Dev Res 2005; 64:1-18.
79. Rost D, Mahner S, Sugiyama Y, Stremmel W. Expression and localization of the multidrug resistance-associated protein 3 in rat small and large intestine. Am J Physiol Gastrointest Liver Physiol 2002; 282:G720-G726.
80. Keppler D, Kamisako T, Leier I, et al. Localization, substrate specificity, and drug resistance conferred by conjugate export pumps of the MRP family. Adv Enzyme Regul 2000; 40:339-349.
81. Keppler D, Cui Y, Konig J, Leier I, Nies A. Export pumps for anionic conjugates encoded by MRP genes. Adv Enzyme Regul 1999; 39:237-246.
82. Glavinas H, Krajcsi P, Cserepes J, Sarkadi B. The role of ABC transporters in drug resistance, metabolism and toxicity. Curr Drug Deliv 2004; 1:27-42.
83. Minich T, Riemer J, Schulz JB, Wielinga P, Wijnholds J, Dringen R. The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J Neurochem 2006; 97:373-384.
84. Pardridge WM, Golden PL, Kang YS Bickel U. Brain microvascular and astrocyte localization of P-glycoprotein. J Neurochem 1997; 68:1278-1285.
85. Karssen AM, Meijer O, Pons D, et al. Localization of mRNA expression of P-glycoprotein at the blood-brain barrier and in the hippocampus. Ann NY Acad Sci 2004; 1032:308-311.
86. Hirsch-Ernst KI, Ziemann C, Schmitz-Salue C, Foth H, Kahl GF. Modulation of P-glycoprotein and mdr1b mRNA expression by growth factors in primary rat hepatocyte culture. Biochem Biophys Res Commun 1995; 215:179-185.
87. Krishnamurthy P, Ross DD, Nakanishi T, et al. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 2004; 279:24218-24225.
88. Krishnamurthy P, Schuetz JD. The ABC transporter Abcg2/Bcrp: role in hypoxia mediated survival. Biometals 2005; 18:349-358.
89. Mao Q, Unadkat JD. Role of the breast cancer resistance protein (ABCG2) in drug transport. AAPS J 2005; 7:E118-E133.
90. Sarkadi B, Ozvegy-Laczka C, Nemet K, Varadi A. ABCG2 - a transporter for all seasons. FEBS Lett 2004; 567:116-120.
91. Marchi N, Hallene KL, Kight KM, et al. Significance of MDR1 and multiple drug resistance in refractory human epileptic brain. BMC Med 2004; 2:37.
92. Liang XJ, Aszalos A. Multidrug transporters as drug targets. Curr Drug Targets 2006; 7:911-921.
93. Israeli D, Ziaei S, Gonin P, et al. A proposal for the physiological significance of mdr1 and Bcrp1/Abcg2 gene expression in normal tissue regeneration and after cancer therapy. J Theor Biol 2005; 232:41-45.
94. Nakatsukasa H, Silverman JA, Gant TW, et al. Expression of multidrug resistance genes in rat liver during regeneration and after carbon tetrachloride intoxication. Hepatology 1993; 18:1202-1207.
95. Teeter LD, Becker FF, Chisari FV, et al. Overexpression of the multidrug resistance gene mdr3 in spontaneous and chemically induced mouse hepatocellular carcinomas. Mol Cell Biol 1990; 10:5728-5735.
96. Hirsch-Ernst KI, Ziemann C, Foth H, et al. Induction of mdr1b mRNA and P-glycoprotein expression by tumor necrosis factor alpha in primary rat hepatocyte cultures. J Cell Physiol 1998; 176:506-515.
97. Lazarowski A, Ramos AJ, Garcia-Rivello H, et al. Neuronal and glial expression of the multidrug resistance gene product in an experimental epilepsy model. Cell Mol Neurobiol 2004; 24:77-85.
98. Ramos AJ, Lazarowski A, Villar MJ, et al. Transient expression of MDR-1/P-glycoprotein in a model of partial cortical devascularization. Cell Mol Neurobiol 2004; 24:101-107.
99. Volk HA, Burkhardt K, Potschka H, et al. Neuronal expression of the drug efflux transporter P-glycoprotein in the rat hippocampus after limbic seizures. Neuroscience 2004; 123:751-759.
100. Yang JM, Sullivan GF, Hait WN. Regulation of the function of P-glycoprotein by epidermal growth factor through phospholipase C. Biochem Pharmacol 1997; 53:1597-1604.
101. Nies AT, Jedlitschky G, Konig J, et al. Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 2004; 129:349-360.
102. Hirrlinger J, Moeller H, Kirchhoff F, Dringen R. Expression of multidrug resistance proteins (Mrps) in astrocytes of the mouse brain: a single cell RT-PCR study. Neurochem Res 2005; 30:1237-1244.
103. Hirrlinger J, Konig J, Dringen R. Expression of mRNAs of multidrug resistance proteins (Mrps) in cultured rat astrocytes, oligodendrocytes, microglial cells and neurones. J Neurochem 2002; 82:716-719.
104. Dallas S, Miller DS, Bendayan R. Multidrug resistance-associated proteins: expression and function in the central nervous system. Pharmacol Rev 2006; 58:140-161.
105. Kim WS, Guillemin GJ, Glaros EN, Lim CK, Garner B. Quantitation of ATP-binding cassette subfamily-A transporter gene expression in primary human brain cells. Neuroreport 2006; 17:891-896.
106. Hirsch-Reinshagen V, Zhou S, Burgess BL, et al. Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. J Biol Chem 2004; 279:41197-41207.
107. Brewer HB Jr, Remaley AT, Neufeld EB, Basso F, Joyce C. Regulation of plasma high-density lipoprotein levels by the ABCA1 transporter and the emerging role of high-density lipoprotein in the treatment of cardiovascular disease. Arterioscler Thromb Vasc Biol 2004; 24:1755-1760.
108. Le Goff W, Settle M, Greene DJ, Morton RE, Smith JD. Reevaluation of the role of the multidrug-resistant P-glycoprotein in cellular cholesterol homeostasis. J Lipid Res 2006; 47:51-58.
109. Burns MP, Vardanian L, Pajoohesh-Ganji A, et al. The effects of ABCA1 on cholesterol efflux and Abeta levels in vitro and in vivo. J Neurochem 2006; 98:792-800.
110. Fukumoto H, Deng A, Irizarry MC, Fitzgerald ML, Rebeck GW. Induction of the cholesterol transporter ABCA1 in central nervous system cells by liver X receptor agonists increases secreted Abeta levels. J Biol Chem 2002; 277:48508-48513.
111. Wahrle SE, Jiang H, Parsadanian M, et al. Deletion of Abca1 increases Abeta deposition in the PDAPP transgenic mouse model of Alzheimer disease. J Biol Chem 2005; 280:43236-43242.
112. Koldamova R, Staufenbiel M, Lefterov I. Lack of ABCA1 considerably decreases brain ApoE level and increases amyloid deposition in APP23 mice. J Biol Chem 2005; 280:43224-43235.
113. Hirsch-Reinshagen V, Maia LF, Burgess BL, et al. The absence of ABCA1 decreases soluble ApoE levels but does not diminish amyloid deposition in two murine models of Alzheimer disease. J Biol Chem 2005; 280:43243-43256.
114. Karten B, Campenot RB, Vance DE, Vance JE. Expression of ABCG1, but not ABCA1, correlates with cholesterol release by cerebellar astroglia. J Biol Chem 2006; 281:4049-4057.
115. Leonard GD, Fojo T, Bates SE. The role of ABC transporters in clinical practice. Oncologist 2003; 8:411-424.
116. Stefkova J, Poledne R, Hubacek JA. ATP-binding cassette (ABC) transporters in human metabolism and diseases. Physiol Res 2004; 53:235-243.
117. Dean M, Allikmets R. Complete characterization of the human ABC gene family. J Bioenerg Biomembr 2001; 33:475-479.
118. Vergani P, Basso C, Mense M, Nairn AC, Gadsby DC. Control of the CFTR channel's gates. Biochem Soc Trans 2005; 33:1003-1007.
119. McGinniss MJ, Chen C, Redman JB, et al. Extensive sequencing of the CFTR gene: lessons learned from the first 157 patient samples. Hum Genet 2005; 118:331-338.
120. Vander Borght S, Libbrecht L, Katoonizadeh A, et al. Breast cancer resistance protein (BCRP/ABCG2) is expressed by progenitor cells/reactive ductules and hepatocytes and its expression pattern is influenced by disease etiology and species type: possible functional consequences. J Histochem Cytochem 2006; 54:1051-1059.
121. Borst P, Elferink RO. Mammalian ABC transporters in health and disease. Annu Rev Biochem 2002; 71:537-592.
122. Ros JE, Roskams TA, Geuken M, et al. ATP binding cassette transporter gene expression in rat liver progenitor cells. Gut 2003; 52:1060-1067.
123. Ros JE, Libbrecht L, Geuken M, Jansen PL, Roskams TA. High expression of MDR1, MRP1, and MRP3 in the hepatic progenitor cell compartment and hepatocytes in severe human liver disease. J Pathol 2003; 200:553-560.
124. Libbrecht L, Desmet V, Roskams T. Preneoplastic lesions in human hepatocarcinogenesis. Liver Int 2005; 25:16-27.
125. Newsome PN, Hussain MA, Theise ND. Hepatic oval cells: helping redefine a paradigm in stem cell biology. Curr Top Dev Biol 2004; 61:1-28.
126. Inagaki N, Gonoi T, Clement JP IV, et al. Reconstitution of IKATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 1995; 270:1166-1170.
127. Koriyama N, Kakei M, Nakazaki M, et al. PIP2 and ATP cooperatively prevent cytosolic Ca2+-induced modification of ATP-sensitive K+ channels in rat pancreatic beta-cells. Diabetes 2000; 49:1830-1839.
128. Chaudhary PM, Roninson IB. Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells. Cell 1991; 66:85-94.
129. Kim M, Turnquist H, Jackson J, et al. The multidrug resistance transporter ABCG2 (breast cancer resistance protein 1) effluxes Hoechst 33342 and is overexpressed in hematopoietic stem cells. Clin Cancer Res 2002; 8:22-28.
130. Hirschmann-Jax C, Foster AE, Wulf GG, et al. A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 2004; 101:14228-14233.
131. Chiba T, Kita K, Zheng YW, et al. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology 2006; 44:240-251.
132. Fuellen G, Spitzer M, Cullen P, Lorkowski S. Correspondence of function and phylogeny of ABC proteins based on an automated analysis of 20 model protein data sets. Proteins 2005; 61:888-899.
133. Lorkowski S, Cullen P. ABCG subfamily of human ATP-binding cassette proteins. Pure Appl Chem 2002; 74:2057-2081.
134. Mouthon MA, Fouchet P, Mathieu C, et al. Neural stem cells from mouse forebrain are contained in a population distinct from the 'side population'. J Neurochem 2006. Epub ahead of print.
135. Haraguchi N, Utsunomiya T, Inoue H, et al. Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 2006; 24:506-513.
136. Meissner K, Heydrich B, Jedlitschky G, et al. The ATP-binding cassette transporter ABCG2 (BCRP), a marker for side population stem cells, is expressed in human heart. J Histochem Cytochem 2006; 54:215-221.
137. McAlister I, Wolf NS, Pietrzyk ME, et al. Transplantation of hematopoietic stem cells obtained by a combined dye method fractionation of murine bone marrow. Blood 1990; 75:1240-1246.
138. Wolf NS, Kone A, Priestley GV, et al. In vivo and in vitro characterization of long-term repopulating primitive hematopoietic cells isolated by sequential Hoechst 33342-rhodamine 123 FACS selection. Exp Hematol 1993; 21:614-622.
139. Leemhuis T, Yoder MC, Grigsby S, et al. Isolation of primitive human bone marrow hematopoietic progenitor cells using Hoechst 33342 and Rhodamine 123. Exp Hematol 1996; 24:1215-1224.
140. Bunting KD. ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 2002; 20:11-20.
141. Matsuzaki Y, Kinjo K, Mulligan RC, Okano H. Unexpectedly efficient homing capacity of purified murine hematopoietic stem cells. Immunity 2004; 20:87-93.
142. Norwood K, Wang RY, Hirschmann-Jax C, et al. An in vivo propagated human acute myeloid leukemia expressing ABCA3. Leuk Res 2004; 28:295-299.
143. Scharenberg CW, Harkey MA, Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 2002; 99:507-512.
144. Bunting KD, Zhou S, Lu T, et al. Enforced P-glycoprotein pump function in murine bone marrow cells results in expansion of side population stem cells in vitro and repopulating cells in vivo. Blood 2000; 96:902-909.
145. Lechner A, Leech CA, Abraham EJ, et al. Nestin-positive progenitor cells derived from adult human pancreatic islets of Langerhans contain side population (SP) cells defined by expression of the ABCG2 (BCRP1) ATP-binding cassette transporter. Biochem Biophys Res Commun 2002; 293:670-674.
146. Kawanabe N, Murakami K, Takano-Yamamoto T. The presence of ABCG2-dependent side population cells in human periodontal ligaments. Biochem Biophys Res Commun 2006; 344:1278-1283.
147. Zhou S, Morris JJ, Barnes Y, et al. Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc Natl Acad Sci USA 2002; 99:12339-12344.
148. Naylor CS, Jaworska E, Branson K, Embleton MJ, Chopra R. Side population/ABCG2-positive cells represent a heterogeneous group of haemopoietic cells: implications for the use of adult stem cells in transplantation and plasticity protocols. Bone Marrow Transplant 2005; 35:353-360.
149. Ueda T, Brenner S, Malech HL, et al. Cloning and functional analysis of the rhesus macaque ABCG2 gene. Forced expression confers an SP phenotype among hematopoietic stem cell progeny in vivo. J Biol Chem 2005; 280:991-998.
150. Jonker JW, Freeman J, Bolscher E, et al. Contribution of the ABC transporters Bcrp1 and Mdr1a/1b to the side population phenotype in mammary gland and bone marrow of mice. Stem Cells 2005; 23:1059-1065.
151. Challen GA, Little MH. A side order of stem cells: the SP phenotype. Stem Cells 2006; 24:3-12.
152. Scharenberg CW, Harkey MA, Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 2002; 99:507-512.
153. Konya A, Andor A, Satorhelyi P, Nemeth K, Kurucz I. Inhibition of the MDR1 transporter by new phenothiazine derivatives. Biochem Biophys Res Commun 2006; 346:45-50.
154. Ogihara T, Kamiya M, Ozawa M, et al. What kinds of substrates show P-glycoprotein-dependent intestinal absorption? Comparison of verapamil with vinblastine. Drug Metab Pharmacokinet 2006; 21:238-244.
155. Zhou S, Schuetz JD, Bunting KD, et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 2001; 7:1028-1034.
156. Tadjali M, Zhou S, Rehg J, Sorrentino BP. Prospective isolation of murine hematopoietic stem cells by expression of an Abcg2/GFP allele. Stem Cells 2006; 24:1556-1563.
157. Chen CJ, Chin JE, Ueda K, et al. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 1986; 47:381-389.
158. Gros P, Croop J, Housman D. Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell 1986; 47:371-380.
159. Hsu SI, Lothstein L, Horwitz SB. Differential overexpression of three mdr gene family members in multidrug-resistant J774.2 mouse cells. Evidence that distinct P-glycoprotein precursors are encoded by unique mdr genes. J Biol Chem 1989; 264:12053-12062.
160. Devault A, Gros P. Two members of the mouse mdr gene family confer multidrug resistance with overlapping but distinct drug specificities. Mol Cell Biol 1990; 10:1652-1663.
161. Wang EJ, Casciano CN, Clement RP, Johnson WW. Active transport of fluorescent P-glycoprotein substrates: evaluation as markers and interaction with inhibitors. Biochem Biophys Res Commun 2001; 289:580-585.
162. Schinkel AH, Smit JJ, van Tellingen O, et al. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 1994; 77:491-502.
163. Schinkel AH, Mayer U, Wagenaar E, et al. Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins. Proc Natl Acad Sci USA 1997; 94:4028-4033.
164. Zhou S, Zong Y, Lu T, et al. Hematopoietic cells from mice that are deficient in both Bcrp1/Abcg2 and Mdr1a/1b develop normally but are sensitized to mitoxantrone. Biotechniques 2003; 35:1248-1252.
165. Panwala CM, Jones JC, Viney JL. A novel model of inflammatory bowel disease: mice deficient for the multiple drug resistance gene, mdr1a, spontaneously develop colitis. J Immunol 1998; 161:5733-5744.
166. Broccardo C, Nieoullon V, Amin R, et al. ABCA2 is a marker of neural progenitors and neuronal subsets in the adult rodent brain. J Neurochem 2006; 97:345-355.
167. Islam MO, Kanemura Y, Tajria J, et al. Characterization of ABC transporter ABCB1 expressed in human neural stem/progenitor cells. FEBS Lett 2005; 579:3473-3480.
168. Islam MO, Kanemura Y, Tajria J, et al. Functional expression of ABCG2 transporter in human neural stem/progenitor cells. Neurosci Res 2005; 52:75-82.
169. Suslov ON, Kukekov VG, Ignatova TN, et al. Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proc Natl Acad Sci USA 2002; 99:14506-14511.
170. Alison MR. Tissue-based stem cells: ABC transporter proteins take centre stage. J Pathol 2003; 21:547-550.
171. Roitberg BZ, Mangubat E, Chen EY, et al. Survival and early differentiation of human neural stem cells transplanted in a nonhuman primate model of stroke. J Neurosurg 2006; 105:96-102.
172. Cummings BJ, Uchida N, Tamaki SJ, Anderson AJ. Human neural stem cell differentiation following transplantation into spinal cord injured mice: association with recovery of locomotor function. Neurol Res 2006; 28:474-481.
173. Watson DJ, Walton RM, Magnitsky SG, Bulte JW, Poptani H, Wolfe JH. Structure-specific patterns of neural stem cell engraftment after transplantation in the adult mouse brain. Hum Gene Ther 2006; 17:693-704.
174. Park KI, Himes BT, Stieg PE, Tessler A, Fischer I, Snyder EY. Neural stem cells may be uniquely suited for combined gene therapy and cell replacement: Evidence from engraftment of Neurotrophin-3-expressing stem cells in hypoxic-ischemic brain injury. Exp Neurol 2006; 199:179-190.
175. Shindo T, Matsumoto Y, Wang Q, Kawai N, Tamiya T, Nagao S. Differences in the neuronal stem cells survival, neuronal differentiation and neurological improvement after transplantation of neural stem cells between mild and severe experimental traumatic brain injury. J Med Invest 2006; 53:42-51.
176. Wang Q, Matsumoto Y, Shindo T, et al. Neural stem cells transplantation in cortex in a mouse model of Alzheimer's disease. J Med Invest 2006; 53:61-69.
177. Sugaya K, Alvarez A, Marutle A, Kwak YD, Choumkina E. Stem cell strategies for Alzheimer's disease therapy. Panminerva Med 2006; 48:87-96.
178. Garbossa D, Fontanella M, Fronda C, et al. New strategies for repairing the injured spinal cord: the role of stem cells. Neurol Res 2006; 28:500-504.
179. Martino G, Pluchino S. The therapeutic potential of neural stem cells. Nat Rev Neurosci 2006; 7:395-406.
180. Heese K, Akatsu H. Alzheimer's disease - an interactive perspective. Curr Alzheimer Res 2006; 3:109-121.
181. Sugaya K. Possible use of autologous stem cell therapies for Alzheimer's disease. Curr Alzheimer Res 2005; 2:367-376.