Human cerebrospinal fluid regulates proliferation and migration of stem cells through insulin-like growth factor-1

Stem Cells and Development

Volumn 24, Issue 2, 2015, Pages 160-171

  Zhu, Mingxin ^a,b   Feng, Yun ^a,c   Dangelmajer, Sean ^a   Guerrero Cázares, Hugo ^a   Chaichana, Kaisorn L ^a   Smith, Christopher L ^a   Levchenko, Andre ^d   Lei, Ting ^b   Quinoñes Hinojosa, Alfredo ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c JIANGSU UNIVERSITY   (China)

^d Yale University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; SOMATOMEDIN C; CXCR4 PROTEIN, HUMAN;

ADIPOSE DERIVED STEM CELL; ADOLESCENT; ADULT; AGED; APOPTOSIS; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CEREBROSPINAL FLUID; CHILD; CLINICAL ARTICLE; COMMUNICATING HYDROCEPHALUS; CONGENITAL HYDROCEPHALUS; CONTROLLED STUDY; CULTURE MEDIUM; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN ADIPOSE DERIVED MESENCHYMAL STEM CELL; HUMAN CELL; HUMAN FETAL DERIVED NEURAL PROGENITOR CELL; IMMUNOHISTOCHEMISTRY; MALE; MESENCHYMAL STEM CELL; MIDDLE AGED; MTT ASSAY; NEURAL STEM CELL; NORMOTENSIVE HYDROCEPHALUS; OBSTRUCTIVE HYDROCEPHALUS; PRESCHOOL CHILD; PRIORITY JOURNAL; REGULATORY MECHANISM; YOUNG ADULT; BIOSYNTHESIS; CELL MOTION; CYTOLOGY; EVALUATION STUDY; GENE EXPRESSION REGULATION; MESENCHYMAL STROMA CELL; METABOLISM; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CEREBROSPINAL FLUID; GENE EXPRESSION REGULATION; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MESENCHYMAL STROMAL CELLS; NEURAL STEM CELLS; RECEPTORS, CXCR4;

EID: 84920806789     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0076     Document Type: Article

References (57)

1. Titomanlio L, A Kavelaars, J Dalous, S Mani, V El Ghouzzi, C Heijnen, O Baud and P Gressens. (2011). Stem cell therapy for neonatal brain injury: perspectives and challenges. Ann Neurol 70:698-712.
2. Aboody KS, J Najbauer and MK Danks. (2008). Stem and progenitor cell-mediated tumor selective gene therapy. Gene Ther 15:739-752.
3. Trounson A, RG Thakar, G Lomax and D Gibbons. (2011). Clinical trials for stem cell therapies. BMC Med 9:52.
4. Karp JM and GS Leng Teo. (2009). Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4:206-216.
5. Nakamizo A, F Marini, T Amano, A Khan, M Studeny, J Gumin, J Chen, S Hentschel, G Vecil, et al. (2005). Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res 65:3307-3318.
6. Bachoud-Levi AC, V Gaura, P Brugieres, JP Lefaucheur, MF Boisse, P Maison, S Baudic, MJ Ribeiro, C Bourdet, et al. (2006). Effect of fetal neural transplants in patients with Huntington's disease 6 years after surgery: a long-term follow-up study. Lancet Neurol 5:303-309.
7. Benedetti S, B Pirola, B Pollo, L Magrassi, MG Bruzzone, D Rigamonti, R Galli, S Selleri, MF Di, et al. (2000). Gene therapy of experimental brain tumors using neural progenitor cells. Nat Med 6:447-450.
8. Lee DH,Y Ahn, SU Kim,KC Wang,BK Cho, JH Phi, IH Park, PM Black,RSCarroll, JLee and SKKim. (2009).Targeting rat brainstem glioma using human neural stem cells and human mesenchymal stem cells. Clin Cancer Res 15:4925-4934.
9. Lee C and DV Agoston. (2010). Vascular endothelial growth factor is involved in mediating increased de novo hippocampal neurogenesis in response to traumatic brain injury. J Neurotrauma 27:541-553.
10. Guan J, Z Zhu, RC Zhao, Z Xiao, C Wu, Q Han, L Chen,W Tong, J Zhang, et al. (2013). Transplantation of human mesenchymal stem cells loaded on collagen scaffolds for the treatment of traumatic brain injury in rats. Biomaterials 34:5937-5946.
11. van Velthoven CT, RA Sheldon, A Kavelaars, N Derugin, ZS Vexler, HLWillemen,MMaas, CJ Heijnen andDMFerriero. (2013). Mesenchymal stem cell transplantation attenuates brain injury after neonatal stroke. Stroke 44:1426-1432.
12. Zappaterra MW and MK Lehtinen. (2012). The cerebrospinal fluid: regulator of neurogenesis, behavior, and beyond. Cell Mol Life Sci 69:2863-2878.
13. Johanson CE, JA Duncan, EG Stopa and A Baird. (2005). Enhanced prospects for drug delivery and brain targeting by the choroid plexus-CSF route. Pharm Res 22:1011-1037.
14. Lehtinen MK and CA Walsh. (2011). Neurogenesis at the brain-cerebrospinal fluid interface. Annu Rev Cell Dev Biol 27:653-679.
15. Lehtinen MK, MW Zappaterra, X Chen, YJ Yang, AD Hill, M Lun, T Maynard, D Gonzalez, S Kim, et al. (2011). The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 69:893-905.
16. Cristofanilli M, B Cymring, A Lu, H Rosenthal and SA Sadiq. (2013). Cerebrospinal fluid derived from progressive multiple sclerosis patients promotes neuronal and oligodendroglial differentiation of human neural precursor cells in vitro. Neuroscience 250:614-621.
17. Buddensiek J, A Dressel, M Kowalski, U Runge, H Schroeder, A Hermann, M Kirsch, A Storch and M Sabolek. (2010). Cerebrospinal fluid promotes survival and astroglial differentiation of adult human neural progenitor cells but inhibits proliferation and neuronal differentiation. BMC Neurosci 11:48.
18. Benarroch EE. (2012). Insulin-like growth factors in the brain and their potential clinical implications. Neurology 79:2148-2153.
19. Liu W, P Ye, JR O'Kusky and AJ D'Ercole. (2009). Type 1 insulin-like growth factor receptor signaling is essential for the development of the hippocampal formation and dentate gyrus. J Neurosci Res 87:2821-2832.
20. Ponte AL, E Marais, N Gallay, A Langonne, B Delorme, O Herault, P Charbord and J Domenech. (2007). The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25:1737-1745.
21. Pendleton C, Q Li, DA Chesler, K Yuan, H Guerrero-Cazares and A Quinones-Hinojosa. (2013). Mesenchymal stem cells derived from adipose tissue vs bone marrow: in vitro comparison of their tropismtowards gliomas. PLoSOne 8:e58198.
22. Chaichana KL, H Guerrero-Cazares, V Capilla-Gonzalez, G Zamora-Berridi, P Achanta, O Gonzalez-Perez, GI Jallo, JM Garcia-Verdugo and A Quinones-Hinojosa. (2009). Intra-operatively obtained human tissue: protocols and techniques for the study of neural stem cells. J Neurosci Methods 180:116-125.
23. Guerrero-Cazares H, KL Chaichana and A Quinones-Hinojosa. (2009). Neurosphere culture and human organotypic model to evaluate brain tumor stem cells. Methods Mol Biol 568:73-83.
24. Tzeng SY, H Guerrero-Cazares, EE Martinez, JC Sunshine, A Quinones-Hinojosa and JJ Green. (2011). Non-viral gene delivery nanoparticles based on poly(beta-amino esters) for treatment of glioblastoma. Biomaterials 32:5402-5410.
25. Verkuyl JM and A Matus. (2006). Time-lapse imaging of dendritic spines in vitro. Nat Protoc 1:2399-2405.
26. Kiiski H, R Aanismaa, J Tenhunen, S Hagman, L Yla-Outinen, A Aho, A Yli-Hankala, S Bendel, H Skottman and S Narkilahti. (2013). Healthy human CSF promotes glial differentiation of hESC-derived neural cells while retaining spontaneous activity in existing neuronal networks. Biol Open 2:605-612.
27. Imitola J, K Raddassi, KI Park, FJ Mueller, M Nieto, YD Teng, D Frenkel, J Li, RL Sidman, et al. (2004). Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci USA 101:18117-18122.
28. Kahn J, T Byk, L Jansson-Sjostrand, I Petit, S Shivtiel, A Nagler, I Hardan, V Deutsch, Z Gazit, et al. (2004). Overexpression of CXCR4 on human CD34 + progenitors increases their proliferation, migration, and NOD/SCID repopulation. Blood 103:2942-2949.
29. Kim DH, PP Provenzano, CL Smith and A Levchenko. (2012). Matrix nanotopography as a regulator of cell function. J Cell Biol 197:351-360.
30. Garzon-Muvdi T, P Schiapparelli, C ap Rhys, H Guerrero-Cazares, C Smith, DH Kim, L Kone, H Farber, DY Lee, et al. (2012). Regulation of brain tumor dispersal by NKCC1 through a novel role in focal adhesion regulation. PLoS Biol 10:e1001320.
31. Lehtinen MK, CS Bjornsson, SM Dymecki, RJ Gilbertson, DM Holtzman and ES Monuki. (2013). The choroid plexus and cerebrospinal fluid: emerging roles in development, disease, and therapy. J Neurosci 33:17553-17559.
32. Angot E, K Loulier, KT Nguyen-Ba-Charvet, AP Gadeau, M Ruat and E Traiffort. (2008). Chemoattractive activity of sonic hedgehog in the adult subventricular zone modulates the number of neural precursors reaching the olfactory bulb. Stem Cells 26:2311-2320.
33. Castells A, M Parvas and D Bueno. (2012). Homeostasis of cerebrospinal fluid has a role in early brain development. Neuroreport 23:917-921.
34. Bunn RC, WD King, MK Winkler and JL Fowlkes. (2005). Early developmental changes in IGF-I, IGF-II, IGF binding protein-1, and IGF binding protein-3 concentration in the cerebrospinal fluid of children. Pediatr Res 58:89-93.
35. Aboody KS, A Brown, NG Rainov, KA Bower, S Liu, W Yang, JE Small, U Herrlinger, V Ourednik, et al. (2000). Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 97:12846-12851.
36. Kim SK, SU Kim, IH Park, JH Bang, KS Aboody, KC Wang, BK Cho, M Kim, LG Menon, PM Black and RS Carroll. (2006). Human neural stem cells target experimental intracranial medulloblastoma and deliver a therapeutic gene leading to tumor regression. Clin Cancer Res 12:5550-5556.
37. Amariglio N, A Hirshberg, BW Scheithauer, Y Cohen, R Loewenthal, L Trakhtenbrot, N Paz, M Koren-Michowitz, D Waldman, et al. (2009). Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med 6:e1000029.
38. Aboody KS, J Najbauer,MZMetz, M D'Apuzzo, M Gutova, AJ Annala, TW Synold, LA Couture, S Blanchard, et al. (2013). Neural stem cell-mediated enzyme/prodrug therapy for glioma: preclinical studies. Sci Transl Med 5:184ra59.
39. Li Q, O Wijesekera, SJ Salas, JY Wang, M Zhu, C Aprhys, KL Chaichana, DA Chesler, H Zhang, et al. (2014). Mesenchymal stem cells from human fat engineered to secrete BMP4 are nononcogenic, suppress brain cancer, and prolong survival. Clin Cancer Res 20:2375-2387.
40. Zhu M, K Shu,H Wang,X Li, Q Xiao,W Chan, B Emmanuel, W Jiang and T Lei. (2013). Microtransplantation of whole ganglionic eminence cells ameliorates motor deficit, enlarges the volume of grafts, and prolongs survival in a rat model of Huntington's disease. J Neurosci Res 91:1563-1571.
41. Ma L, B Hu, Y Liu, SC Vermilyea, H Liu, L Gao, Y Sun, X Zhang and SC Zhang. (2012). Human embryonic stem cellderived GABA neurons correct locomotion deficits in quinolinic acid-lesioned mice. Cell Stem Cell 10:455-464.
42. Yang B, X Xi, J Aronowski and SI Savitz. (2012). Ischemic stroke may activate bone marrow mononuclear cells to enhance recovery after stroke. Stem Cells Dev 21:3332-3340.
43. Chavakis E, C Urbich and S Dimmeler. (2008). Homing and engraftment of progenitor cells: a prerequisite for cell therapy. J Mol Cell Cardiol 45:514-522.
44. Zhang D, GC Fan, X Zhou, T Zhao, Z Pasha, M Xu, Y Zhu, M Ashraf and Y Wang. (2008). Over-expression of CXCR4 on mesenchymal stem cells augments myoangiogenesis in the infarcted myocardium. J Mol Cell Cardiol 44:281-292.
45. Chen W, M Li, H Cheng, Z Yan, J Cao, B Pan, W Sang, Q Wu, L Zeng, Z Li and K Xu. (2013). Overexpression of the mesenchymal stem cell Cxcr4 gene in irradiated mice increases the homing capacity of these cells. Cell Biochem Biophys 67:1181-1191.
46. Kim DS, JH Kim, JK Lee, SJ Choi, JS Kim, SS Jeun, W Oh, YS Yang and JW Chang. (2009). Overexpression of CXC chemokine receptors is required for the superior gliomatracking property of umbilical cord blood-derived mesenchymal stem cells. Stem Cells Dev 18:511-519.
47. Daley GQ and DT Scadden. (2008). Prospects for stem cellbased therapy. Cell 132:544-548.
48. Daley GQ. (2012). The promise and perils of stem cell therapeutics. Cell Stem Cell 10:740-749.
49. Liu JP, J Baker, AS Perkins, EJ Robertson and A Efstratiadis. (1993). Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75:59-72.
50. Joseph DA and P Ye. (2008). Expanding the mind: insulinlike growth factor I and brain development. Endocrinology 149:5958-5962.
51. Bibollet-Bahena O and G Almazan. (2009). IGF-1-stimulated protein synthesis in oligodendrocyte progenitors requires PI3K/mTOR/Akt and MEK/ERK pathways. J Neurochem 109:1440-1451.
52. Hardy KM, TA Yatskievych, J Konieczka, AS Bobbs and PB Antin. (2011). FGF signalling through RAS/MAPK and PI3K pathways regulates cell movement and gene expression in the chicken primitive streak without affecting Ecadherin expression. BMC Dev Biol 11:20.
53. Rafalski VA and A Brunet. (2011). Energy metabolism in adult neural stem cell fate. Prog Neurobiol 93:182-203.
54. Tothova Z, R Kollipara, BJ Huntly, BH Lee,DH Castrillon,DE Cullen, EP McDowell, S Lazo-Kallanian, IR Williams, et al. (2007). FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128:325-339.
55. Maucksch C, AL McGregor, M Yang, RJ Gordon, M Yang and B Connor. (2013). IGF-I redirects doublecortin-positive cell migration in the normal adult rat brain. Neuroscience 241:106-115.
56. Haider HK, S Jiang, NM Idris and M Ashraf. (2008). IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair. Circ Res 103:1300-1308.
57. Loulier K, JD Lathia, V Marthiens, J Relucio, MR Mughal, SC Tang, T Coksaygan, PE Hall, S Chigurupati, et al. (2009). Beta1 integrin maintains integrity of the embryonic neocortical stem cell niche. PLoS Biol 7:e1000176.