Brain vascular pericytes following ischemia have multipotential stem cell activity to differentiate into neural and vascular lineage cells

Stem Cells

Volumn 33, Issue 6, 2015, Pages 1962-1974

  Nakagomi, Takayuki ^a   Kubo, Shuji ^a   Nakano Doi, Akiko ^a   Sakuma, Rika ^a   Lu, Shan ^a,b   Narita, Aya ^a   Kawahara, Maiko ^a,c   Taguchi, Akihiko ^d   Matsuyama, Tomohiro ^a  

^a HYOGO COLLEGE OF MEDICINE   (Japan)

^b HANGZHOU FIRST PEOPLE'S HOSPITAL   (China)

^c KWANSEI GAKUIN UNIVERSITY   (Japan)

^d INSTITUTE OF BIOMEDICAL RESEARCH AND INNOVATION   (Japan)

Author keywords

Blood brain barrier; Ischemia; Neurovascularization; Pericyte; Reprogramming; Stem cell plasticity

Indexed keywords

KRUPPEL LIKE FACTOR 4; TRANSCRIPTION FACTOR SOX2; VASCULOTROPIN;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN PERICYTE; CELL CULTURE; CELL LINEAGE; ENDOTHELIAL PROGENITOR CELL; EPITHELIAL MESENCHYMAL TRANSITION; HEMANGIOBLAST; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MESENCHYME CELL; MOUSE; MULTIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; NUCLEAR REPROGRAMMING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BRAIN; CELL DIFFERENTIATION; CYTOLOGY; ENDOTHELIUM CELL; ISCHEMIA; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PERICYTE; PHYSIOLOGY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; ENDOTHELIAL CELLS; ISCHEMIA; MALE; MICE; MULTIPOTENT STEM CELLS; NEUROGENESIS; PERICYTES;

EID: 84929839390     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1977     Document Type: Article

References (67)

1. Banerjee S, Bhat MA,. Neuron-glial interactions in blood-brain barrier formation. Annu Rev Neurosci 2007; 30: 235-258.
2. Dar A, Domev H, Ben-Yosef O, et al., Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation 2012; 125: 87-99.
3. Klein D, Weisshardt P, Kleff V, et al., Vascular wall-resident CD44+ multipotent stem cells give rise to pericytes and smooth muscle cells and contribute to new vessel maturation. PLoS One 2011; 6: e20540.
4. Dore-Duffy P, Katychev A, Wang X, et al., CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab 2006; 26: 613-624.
5. Birbrair A, Zhang T, Wang ZM, et al., Type-2 pericytes participate in normal and tumoral angiogenesis. Am J Physiol Cell Physiol 2014; 307: C25-38.
6. Birbrair A, Zhang T, Wang ZM, et al., Skeletal muscle pericyte subtypes differ in their differentiation potential. Stem Cell Res 2012; 10: 67-84.
7. Karow M, Sanchez R, Schichor C, et al., Reprogramming of pericyte-derived cells of the adult human brain into induced neuronal cells. Cell Stem Cell 2012; 11: 471-476.
8. Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A,. Oxygen in stem cell biology: A critical component of the stem cell niche. Cell Stem Cell 2010; 7: 150-161.
9. Yoshida Y, Takahashi K, Okita K, et al., Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell 2009; 5: 237-241.
10. Nakagomi T, Taguchi A, Fujimori Y, et al., Isolation and characterization of neural stem/progenitor cells from post-stroke cerebral cortex in mice. Eur J Neurosci 2009; 29: 1842-1852.
11. Nakagomi T, Molnar Z, Nakano-Doi A, et al., Ischemia-induced neural stem/progenitor cells in the pia mater following cortical infarction. Stem Cells Dev 2011; 20: 2037-2051.
12. Ilzecka J,. The structure and function of blood-brain barrier in ischaemic brain stroke process. Ann Univ Mariae Curie Sklodowska Med 1996; 51: 123-127.
13. Nakagomi N, Nakagomi T, Kubo S, et al., Endothelial cells support survival, proliferation, and neuronal differentiation of transplanted adult ischemia-induced neural stem/progenitor cells after cerebral infarction. Stem Cells 2009; 27: 2185-2195.
14. Nakano-Doi A, Nakagomi T, Fujikawa M, et al., Bone marrow mononuclear cells promote proliferation of endogenous neural stem cells through vascular niches after cerebral infarction. Stem Cells 2010; 28: 1292-1302.
15. Nakagomi T, Molnar Z, Taguchi A, et al., Leptomeningeal-derived doublecortin-expressing cells in poststroke brain. Stem Cells Dev 2012; 21: 2350-2354.
16. Nakagomi T, Nakano-Doi A, Matsuyama T,. Leptomeninges: A novel stem cell niche harboring ischemia-induced neural progenitors. Histol Histopathol 2015; 30: 391-399.
17. Ii M, Nishimura H, Sekiguchi H, et al., Concurrent vasculogenesis and neurogenesis from adult neural stem cells. Circ Res 2009; 105: 860-868.
18. Oishi K, Ito-Dufros Y,. Angiogenic potential of CD44+ CD90+ multipotent CNS stem cells in vitro. Biochem Biophys Res Commun 2006; 349: 1065-1072.
19. Kubo S, Seleme MC, Soifer HS, et al., L1 retrotransposition in nondividing and primary human somatic cells. Proc Natl Acad Sci USA 2006; 103: 8036-8041.
20. Yamaoka N, Kawasaki Y, Xu Y, et al., Establishment of in vivo fluorescence imaging in mouse models of malignant mesothelioma. Int J Oncol 2010; 37: 273-279.
21. Etchevers HC, Vincent C, Le Douarin NM, et al., The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 2001; 128: 1059-1068.
22. Caplan AI,. All MSCs are pericytes? Cell Stem Cell 2008; 3: 229-230.
23. Mokry J, Cizkova D, Filip S, et al., Nestin expression by newly formed human blood vessels. Stem Cells Dev 2004; 13: 658-664.
24. Suzuki S, Namiki J, Shibata S, et al., The neural stem/progenitor cell marker nestin is expressed in proliferative endothelial cells, but not in mature vasculature. J Histochem Cytochem 2010; 58: 721-730.
25. Wang CH, Hsieh IC, Chen SJ, et al., VE-Cadherin(low)alpha-smooth muscle actin+ component of vascular progenitor cells correlates with the coronary artery Gensini score. Circ J 2012; 76: 477-484.
26. Zovein AC, Hofmann JJ, Lynch M, et al., Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 2008; 3: 625-636.
27. Lin CS, Lue TF,. Defining vascular stem cells. Stem Cells Dev 2013; 22: 1018-1026.
28. Ferreira LS, Gerecht S, Shieh HF, et al., Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res 2007; 101: 286-294.
29. Gasperini P, Espigol-Frigole G, McCormick PJ, et al., Kaposi sarcoma herpesvirus promotes endothelial-to-mesenchymal transition through Notch-dependent signaling. Cancer Res 2012; 72: 1157-1169.
30. Vodyanik MA, Yu J, Zhang X, et al., A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell 2010; 7: 718-729.
31. Ellis P, Fagan BM, Magness ST, et al., SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci 2004; 26: 148-165.
32. Takata M, Nakagomi T, Kashiwamura S, et al., Glucocorticoid-induced TNF receptor-triggered T cells are key modulators for survival/death of neural stem/progenitor cells induced by ischemic stroke. Cell Death Differ 2012; 19: 756-767.
33. Takahashi K, Tanabe K, Ohnuki M, et al., Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872.
34. Kim JB, Zaehres H, Wu G, et al., Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 2008; 454: 646-650.
35. Thier M, Worsdorfer P, Lakes YB, et al., Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell 2012; 10: 473-479.
36. Ring KL, Tong LM, Balestra ME, et al., Direct reprogramming of mouse and human fibroblasts into multipotent neural stem cells with a single factor. Cell Stem Cell 2012; 11: 100-109.
37. Takemoto T, Uchikawa M, Yoshida M, et al., Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 2011; 470: 394-398.
38. Giorgetti A, Marchetto MC, Li M, et al., Cord blood-derived neuronal cells by ectopic expression of Sox2 and c-Myc. Proc Natl Acad Sci USA 2012; 109: 12556-12561.
39. Cimadamore F, Fishwick K, Giusto E, et al., Human ESC-derived neural crest model reveals a key role for SOX2 in sensory neurogenesis. Cell Stem Cell 2011; 8: 538-551.
40. Samavarchi-Tehrani P, Golipour A, David L, et al., Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 2010; 7: 64-77.
41. Gotte M, Wolf M, Staebler A, et al., Aberrant expression of the pluripotency marker SOX-2 in endometriosis. Fertil Steril 2011; 95: 338-341.
42. Keramari M, Razavi J, Ingman KA, et al., Sox2 is essential for formation of trophectoderm in the preimplantation embryo. PLoS One 2010; 5: e13952.
43. Hsu HT, Wu PR, Chen CJ, et al., High cytoplasmic expression of Kruppel-like factor 4 is an independent prognostic factor of better survival in hepatocellular carcinoma. Int J Mol Sci 2014; 15: 9894-9906.
44. Geisler JP, Geisler HE, Manahan KJ, et al., Nuclear and cytoplasmic c-myc staining in endometrial carcinoma and their relationship to survival. Int J Gynecol Cancer 2004; 14: 133-137.
45. Hale AT, Tian H, Anih E, et al., Endothelial Kruppel-like factor 4 regulates angiogenesis and the notch signaling pathway. J Biol Chem 2014; 289: 12016-12028.
46. Cowan CE, Kohler EE, Dugan TA, et al., Kruppel-like factor-4 transcriptionally regulates VE-cadherin expression and endothelial barrier function. Circ Res 2010; 107: 959-966.
47. Kubota Y, Hirashima M, Kishi K, et al., Leukemia inhibitory factor regulates microvessel density by modulating oxygen-dependent VEGF expression in mice. J Clin Invest 2008; 118: 2393-2403.
48. Luo J, Qiao F, Yin X,. Hypoxia induces FGF2 production by vascular endothelial cells and alters MMP9 and TIMP1 expression in extravillous trophoblasts and their invasiveness in a cocultured model. J Reprod Dev 2011; 57: 84-91.
49. Lendahl U, Zimmerman LB, McKay RD,. CNS stem cells express a new class of intermediate filament protein. Cell 1990; 60: 585-595.
50. Louissaint A, Jr., Rao S, Leventhal C, et al., Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 2002; 34: 945-960.
51. Taguchi A, Soma T, Tanaka H, et al., Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 2004; 114: 330-338.
52. Shen Q, Wang Y, Kokovay E, et al., Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008; 3: 289-300.
53. Ricci-Vitiani L, Pallini R, Biffoni M, et al., Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010; 468: 824-828.
54. Scully S, Francescone R, Faibish M, et al., Transdifferentiation of glioblastoma stem-like cells into mural cells drives vasculogenic mimicry in glioblastomas. J Neurosci 2012; 32: 12950-12960.
55. Wurmser AE, Nakashima K, Summers RG, et al., Cell fusion-independent differentiation of neural stem cells to the endothelial lineage. Nature 2004; 430: 350-356.
56. Prandini MH, Dreher I, Bouillot S, et al., The human VE-cadherin promoter is subjected to organ-specific regulation and is activated in tumour angiogenesis. Oncogene 2005; 24: 2992-3001.
57. Mao XG, Xue XY, Wang L, et al., CDH5 is specifically activated in glioblastoma stemlike cells and contributes to vasculogenic mimicry induced by hypoxia. Neuro Oncol 2013; 15: 865-879.
58. Cheng L, Huang Z, Zhou W, et al., Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 2013; 153: 139-152.
59. Teng L, Labosky PA,. Neural crest stem cells. Adv Exp Med Biol 2006; 589: 206-212.
60. Nagoshi N, Shibata S, Kubota Y, et al., Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2008; 2: 392-403.
61. Nagoshi N, Shibata S, Nakamura M, et al., Neural crest-derived stem cells display a wide variety of characteristics. J Cell Biochem 2009; 107: 1046-1052.
62. Kubota Y, Takubo K, Hirashima M, et al., Isolation and function of mouse tissue resident vascular precursors marked by myelin protein zero. J Exp Med 2011; 208: 949-960.
63. Hendriksen EM, Span PN, Schuuring J, et al., Angiogenesis, hypoxia and VEGF expression during tumour growth in a human xenograft tumour model. Microvasc Res 2009; 77: 96-103.
64. Birnbaum T, Hildebrandt J, Nuebling G, et al., Glioblastoma-dependent differentiation and angiogenic potential of human mesenchymal stem cells in vitro. J Neurooncol 2011; 105: 57-65.
65. Traktuev DO, Merfeld-Clauss S, Li J, et al., A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 2008; 102: 77-85.
66. Rolny C, Nilsson I, Magnusson P, et al., Platelet-derived growth factor receptor-beta promotes early endothelial cell differentiation. Blood 2006; 108: 1877-1886.
67. Tigges U, Hyer EG, Scharf J, et al., FGF2-dependent neovascularization of subcutaneous Matrigel plugs is initiated by bone marrow-derived pericytes and macrophages. Development 2008; 135: 523-532.