Cultured pericytes from human brain show phenotypic and functional differences associated with differential CD90 expression

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Park, Thomas I H ^a   Feisst, Vaughan ^b   Brooks, Anna E S ^b   Rustenhoven, Justin ^a   Monzo, Hector J ^a   Feng, Sheryl X ^a   Mee, Edward W ^c   Bergin, Peter S ^a,c   Oldfield, Robyn ^d   Graham, E Scott ^a   Curtis, Maurice A ^a   Faull, Richard L M ^a   Dunbar, P Rod ^d   Dragunow, Mike ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c AUCKLAND CITY HOSPITAL   (New Zealand)

^d AUCKLAND CITY HOSPITAL   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; THY 1 MEMBRANE GLYCOPROTEIN;

ADULT; BLOOD BRAIN BARRIER; BRAIN; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMAN; MALE; METABOLISM; PERICYTE; PHENOTYPE; YOUNG ADULT;

ADULT; BIOMARKERS; BLOOD-BRAIN BARRIER; BRAIN; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; MALE; PERICYTES; PHENOTYPE; THY-1 ANTIGENS; YOUNG ADULT;

EID: 84971228973     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep26587     Document Type: Article

References (73)

1. Bonkowski, D., Katyshev, V., Balabanov, R. D., Borisov, A., & Dore-Duffy, P. The CNS microvascular pericyte: pericyte-Astrocyte crosstalk in the regulation of tissue survival. Fluids Barriers CNS 8, 8, doi: 2045-8118-8-8 [pii] 10.1186/2045-8118-8-8 (2011
2. Lin, S. L., Kisseleva, T., Brenner, D. A., & Duffield, J. S. Pericytes and perivascular fibroblasts are the primary source of collagenproducing cells in obstructive fibrosis of the kidney. Am J Pathol 173, 1617-1627, doi: S0002-9440(10)61547-7 [pii] 10.2353/ ajpath.2008.080433 (2008
3. Armulik, A., et al. Pericytes regulate the blood-brain barrier. Nature 468, 557-561, doi: nature09522 [pii] 10.1038/nature09522 (2010
4. Blocki, A., et al. Not All MSCs Can Act as Pericytes: Functional In Vitro Assays to Distinguish Pericytes from Other Mesenchymal Stem Cells in Angiogenesis. Stem Cells Dev, doi: 10.1089/scd.2012.0415 (2013
5. Hellstrom, M., et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153, 543-553 (2001
6. Zechariah, A., et al. Vascular Endothelial Growth Factor Promotes Pericyte Coverage of Brain Capillaries, Improves Cerebral Blood Flow During Subsequent Focal Cerebral Ischemia, and Preserves the Metabolic Penumbra. Stroke 44, 1690-1697, doi: STROKEAHA.111.000240 [pii] 10.1161/STROKEAHA.111.000240 (2013
7. Gaengel, K., Genove, G., Armulik, A., & Betsholtz, C. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 29, 630-638, doi: ATVBAHA.107.161521 [pii] 10.1161/ATVBAHA.107.161521 (2009
8. Dore-Duffy, P., et al. Pericyte-mediated vasoconstriction underlies TBI-induced hypoperfusion. Neurol Res 33, 176-186, doi: 10.11 79/016164111X12881719352372 (2011
9. Hill, R. A., et al. Regional Blood Flow in the Normal and Ischemic Brain Is Controlled by Arteriolar Smooth Muscle Cell Contractility and Not by Capillary Pericytes. Neuron 87, 95-110, doi: S0896-6273(15)00514-0 [pii] 10.1016/j.neuron.2015.06.001 (2015
10. Jansson, D., et al. A role for human brain pericytes in neuroinflammation. J Neuroinflammation 11, 104, doi: 1742-2094-11-104 [pii] 10.1186/1742-2094-11-104 (2014
11. Guijarro-Munoz, I., Compte, M., Alvarez-Cienfuegos, A., Alvarez-Vallina, L., & Sanz, L. Lipopolysaccharide activates Toll-like receptor 4 (TLR4)-mediated NF-kappaB signaling pathway and proinflammatory response in human pericytes. J Biol Chem 289, 2457-2468, doi: M113.521161 [pii] 10.1074/jbc.M113.521161 (2014
12. Stark, K., et al. Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct' them with patternrecognition and motility programs. Nat Immunol 14, 41-51, doi: ni.2477 [pii] 10.1038/ni.2477 (2013
13. Ochs, K., et al. Immature mesenchymal stem cell-like pericytes as mediators of immunosuppression in human malignant glioma. J Neuroimmunol 265, 106-116, doi: S0165-5728(13)00253-1 [pii] 10.1016/j.jneuroim.2013.09.011 (2013
14. Dohgu, S., & Banks, W. A. Brain pericytes increase the lipopolysaccharide-enhanced transcytosis of HIV-1 free virus across the in vitro blood-brain barrier: evidence for cytokine-mediated pericyte-endothelial cell crosstalk. Fluids Barriers CNS 10, 23, doi: 2045-8118-10-23 [pii] 10.1186/2045-8118-10-23 (2013
15. Balabanov, R., Beaumont, T., & Dore-Duffy, P. Role of central nervous system microvascular pericytes in activation of antigenprimed splenic T-lymphocytes. J Neurosci Res 55, 578-587, doi: 10.1002/(SICI)1097-4547(19990301)55: 5 3.0.CO; 2-E [pii] (1999
16. Balabanov, R., Washington, R., Wagnerova, J., & Dore-Duffy, P. CNS microvascular pericytes express macrophage-like function, cell surface integrin alpha M, and macrophage marker ED-2. Microvasc Res 52, 127-142, doi: S0026-2862(96)90049-7 [pii] 10.1006/ mvre.1996.0049 (1996
17. Fernandez-Klett, F., et al. Early loss of pericytes and perivascular stromal cell-induced scar formation after stroke. J Cereb Blood Flow Metab 33, 428-439, doi: jcbfm2012187 [pii] 10.1038/jcbfm.2012.187 (2013
18. Goritz, C., et al. A pericyte origin of spinal cord scar tissue. Science 333, 238-242, doi: 333/6039/238 [pii] 10.1126/science.1203165 (2011
19. Greenhalgh, S. N., Iredale, J. P., & Henderson, N. C. Origins of fibrosis: pericytes take centre stage. F1000Prime Rep 5, 37, doi: 10.12703/P5-37 37 [pii] (2013
20. Lv, F. J., Tuan, R. S., Cheung, K. M., & Leung, V. Y. The surface markers and identity of human mesenchymal stem cells. Stem Cells, doi: 10.1002/stem.1681 (2014
21. Phipps, R. P., et al. Characterization of two major populations of lung fibroblasts: distinguishing morphology and discordant display of Thy 1 and class II MHC. Am J Respir Cell Mol Biol 1, 65-74, doi: 10.1165/ajrcmb/1.1.65 (1989
22. Soderblom, C., et al. Perivascular fibroblasts form the fibrotic scar after contusive spinal cord injury. J Neurosci 33, 13882-13887, doi: 33/34/13882 [pii] 10.1523/JNEUROSCI.2524-13.2013 (2013
23. Xue, G. P., Rivero, B. P., & Morris, R. J. The surface glycoprotein Thy-1 is excluded from growing axons during development: a study of the expression of Thy-1 during axogenesis in hippocampus and hindbrain. Development 112, 161-176 (1991
24. Kisselbach, L., Merges, M., Bossie, A., & Boyd, A. CD90 Expression on human primary cells and elimination of contaminating fibroblasts from cell cultures. Cytotechnology 59, 31-44, doi: 10.1007/s10616-009-9190-3 (2009
25. Feisst, V., Brooks, A. E., Chen, C. J., & Dunbar, P. R. Characterization of mesenchymal progenitor cell populations directly derived from human dermis. Stem Cells Dev 23, 631-642, doi: 10.1089/scd.2013.0207 (2014
26. Mahanthappa, N. K., & Patterson, P. H. Thy-1 involvement in neurite outgrowth: perturbation by antibodies, phospholipase C, and mutation. Dev Biol 150, 47-59, doi: 0012-1606(92)90006-3 [pii] (1992
27. Yang, S. H., et al. Anti-Thy-1 antibody-induced neurite outgrowth in cultured dorsal root ganglionic neurons is mediated by the c-Src-MEK signaling pathway. J Cell Biochem 103, 67-77, doi: 10.1002/jcb.21387 (2008
28. Saalbach, A., Haustein, U. F., & Anderegg, U. A ligand of human thy-1 is localized on polymorphonuclear leukocytes and monocytes and mediates the binding to activated thy-1-positive microvascular endothelial cells and fibroblasts. J Invest Dermatol 115, 882-888, doi: jid104 [pii] 10.1046/j.1523-1747.2000.00104.x (2000
29. Barker, T. H., et al. Thy-1 regulates fibroblast focal adhesions, cytoskeletal organization and migration through modulation of p190 RhoGAP and Rho GTPase activity. Exp Cell Res 295, 488-496, doi: 10.1016/j.yexcr.2004.01.026 S0014482704000680 [pii] (2004
30. Hagood, J. S., et al. Loss of fibroblast Thy-1 expression correlates with lung fibrogenesis. Am J Pathol 167, 365-379, doi: S0002-9440(10)62982-3 [pii] 10.1016/S0002-9440(10)62982-3 (2005
31. Dudas, J., Mansuroglu, T., Batusic, D., & Ramadori, G. Thy-1 is expressed in myofibroblasts but not found in hepatic stellate cells following liver injury. Histochem Cell Biol 131, 115-127, doi: 10.1007/s00418-008-0503-y (2009
32. He, J., et al. CD90 is identified as a candidate marker for cancer stem cells in primary high-grade gliomas using tissue microarrays. Mol Cell Proteomics 11, M111 010744, doi: M111.010744 [pii] 10.1074/mcp.M111.010744 (2012
33. Yang, Z. F., et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13, 153-166, doi: S1535-6108(08)00009-3 [pii] 10.1016/j.ccr.2008.01.013 (2008
34. Zhu, J., Thakolwiboon, S., Liu, X., Zhang, M., & Lubman, D. M. Overexpression of CD90 (Thy-1) in Pancreatic Adenocarcinoma Present in the Tumor Microenvironment. PLos One 9, e115507, doi: 10.1371/journal.pone.0115507 PONE-D-14-35661 [pii] (2014
35. Yamashita, T., et al. Discrete nature of EpCAM+ and CD90+ cancer stem cells in human hepatocellular carcinoma. Hepatology 57, 1484-1497, doi: 10.1002/hep.26168 (2013
36. Tang, K. H., et al. A CD90(+ ) tumor-initiating cell population with an aggressive signature and metastatic capacity in esophageal cancer. Cancer Res 73, 2322-2332, doi: 0008-5472.CAN-12-2991 [pii] 10.1158/0008-5472.CAN-12-2991 (2013
37. Kim, Y. G., et al. Existence of glioma stroma mesenchymal stemlike cells in Korean glioma specimens. Childs Nerv Syst 29, 549-563, doi: 10.1007/s00381-012-1988-1 (2013
38. Takeda, H., Yamamoto, M., Morita, N., & Tanizawa, T. Relationship between Thy-1 expression and cell-cycle distribution in human bone marrow hematopoietic progenitors. Am J Hematol 79, 187-193, doi: 10.1002/ajh.20362 (2005
39. Seita, J., & Weissman, I. L. Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip Rev Syst Biol Med 2, 640-653, doi: 10.1002/wsbm.86 (2010
40. Rege, T. A., & Hagood, J. S. Thy-1, a versatile modulator of signaling affecting cellular adhesion, proliferation, survival, and cytokine/ growth factor responses. Biochim Biophys Acta 1763, 991-999, doi: S0167-4889(06)00223-0 [pii] 10.1016/j.bbamcr.2006.08.008 (2006
41. Nakamura, Y., et al. Expression of CD90 on keratinocyte stem/progenitor cells. Br J Dermatol 154, 1062-1070, doi: BJD7209 [pii] 10.1111/j.1365-2133.2006.07209.x (2006
42. Winkler, E. A., Bell, R. D., & Zlokovic, B. V. Central nervous system pericytes in health and disease. Nat Neurosci 14, 1398-1405, doi: nn.2946 [pii] 10.1038/nn.2946 (2011
43. Paul, G., et al. The adult human brain harbors multipotent perivascular mesenchymal stem cells. PLos One 7, e35577, doi: 10.1371/ journal.pone.0035577 PONE-D-11-11140 [pii] (2012
44. Smith, A. M., Gibbons, H. M., Lill, C., Faull, R. L., & Dragunow, M. Isolation and culture of adult human microglia within mixed glial cultures for functional experimentation and high-content analysis. Methods Mol Biol 1041, 41-51, doi: 10.1007/978-1-62703-520-0-6 (2013
45. Strutz, F., et al. Identification and characterization of a fibroblast marker: FSP1. J Cell Biol 130, 393-405 (1995
46. Paulsson, M. Basement membrane proteins: structure, assembly, and cellular interactions. Crit Rev Biochem Mol Biol 27, 93-127, doi: 10.3109/10409239209082560 (1992
47. Thyberg, J., & Hultgardh-Nilsson, A. Fibronectin and the basement membrane components laminin and collagen type IV influence the phenotypic properties of subcultured rat aortic smooth muscle cells differently. Cell Tissue Res 276, 263-271 (1994
48. Crisan, M., et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3, 301-313, doi: S1934-5909(08)00337-8 [pii] 10.1016/j.stem.2008.07.003 (2008
49. Sieczkiewicz, G. J., & Herman, I. M. TGF-beta 1 signaling controls retinal pericyte contractile protein expression. Microvasc Res 66, 190-196, doi: S0026286203000554 [pii] (2003
50. Vesey, D. A., et al. Interleukin-1beta stimulates human renal fibroblast proliferation and matrix protein production by means of a transforming growth factor-beta-dependent mechanism. J Lab Clin Med 140, 342-350, doi: 10.1067/mlc.2002.128468 S0022214302000902 [pii] (2002
51. Hirschi, K. K., Rohovsky, S. A., & D'Amore, P. A. PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cellinduced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 141, 805-814 (1998
52. Hellstrom, M., Kalen, M., Lindahl, P., Abramsson, A., & Betsholtz, C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126, 3047-3055 (1999
53. Abramsson, A., Lindblom, P., & Betsholtz, C. Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J Clin Invest 112, 1142-1151, doi: 10.1172/JCI18549 112/8/1142 [pii] (2003
54. Kovac, A., Erickson, M. A., & Banks, W. A. Brain microvascular pericytes are immunoactive in culture: cytokine, chemokine, nitric oxide, and LRP-1 expression in response to lipopolysaccharide. J Neuroinflammation 8, 139, doi: 1742-2094-8-139 [pii] 10.1186/1742-2094-8-139 (2011
55. Witkowska, A. M. Soluble ICAM-1: a marker of vascular inflammation and lifestyle. Cytokine 31, 127-134, doi: S1043-4666(05)00138-9 [pii] 10.1016/j.cyto.2005.04.007 (2005
56. Dore-Duffy, P., & LaManna, J. C. Physiologic angiodynamics in the brain. Antioxid Redox Signal 9, 1363-1371, doi: 10.1089/ ars.2007.1713 (2007
57. Zouani, O. F., Lei, Y., & Durrieu, M. C. Pericytes, Stem-Cell-Like Cells, but not Mesenchymal Stem Cells are Recruited to Support Microvascular Tube Stabilization. Small, doi: 10.1002/smll.201300124 (2013
58. Murfee, W. L., Skalak, T. C., & Peirce, S. M. Differential arterial/venous expression of NG2 proteoglycan in perivascular cells along microvessels: identifying a venule-specific phenotype. Microcirculation 12, 151-160, doi: N341R34632273112 [pii] 10.1080/ 10739680590904955 (2005
59. Zhou, C., et al. Effects of human marrow stromal cells on activation of microglial cells and production of inflammatory factors induced by lipopolysaccharide. Brain Res 1269, 23-30, doi: S0006-8993(09)00419-3 [pii] 10.1016/j.brainres.2009.02.049 (2009
60. Walshe, T. E., et al. TGF-beta is required for vascular barrier function, endothelial survival and homeostasis of the adult microvasculature. PLos One 4, e5149, doi: 10.1371/journal.pone.0005149 (2009
61. Wan, M., et al. Injury-Activated transforming growth factor beta controls mobilization of mesenchymal stem cells for tissue remodeling. Stem Cells 30, 2498-2511, doi: 10.1002/stem.1208 (2012
62. Henderson, N. C., & Sheppard, D. Integrin-mediated regulation of TGFbeta in fibrosis. Biochim Biophys Acta 1832, 891-896, doi: S0925-4439(12)00228-1 [pii] 10.1016/j.bbadis.2012.10.005 (2013
63. Wynn, T. A., & Ramalingam, T. R. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 18, 1028-1040, doi: nm.2807 [pii] 10.1038/nm.2807 (2012
64. Ghosh, D., et al. Integral role of platelet-derived growth factor in mediating transforming growth factor-beta1-dependent mesenchymal stem cell stiffening. Stem Cells Dev 23, 245-261, doi: 10.1089/scd.2013.0240 (2014
65. Humphreys, B. D., et al. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 176, 85-97, doi: S0002-9440(10)60327-6 [pii] 10.2353/ajpath.2010.090517 (2010
66. Okamoto, T., et al. Transforming growth factor-beta1 induces matrix metalloproteinase-9 expression in human meningeal cells via ERK and Smad pathways. Biochem Biophys Res Commun 383, 475-479, doi: S0006-291X(09)00727-X [pii] 10.1016/j. bbrc.2009.04.038 (2009
67. Alon, R., & Nourshargh, S. Learning in motion: pericytes instruct migrating innate leukocytes. Nat Immunol 14, 14-15, doi: ni.2489 pii] 10.1038/ni.2489 (2013).
68. Loibl, M., et al. Direct Cell-Cell Contact between Mesenchymal Stem Cells and Endothelial Progenitor Cells Induces a Pericyte-Like Phenotype In Vitro. Biomed Res Int 2014, 395781, doi: 10.1155/2014/395781 (2014
69. Shan, B., et al. Thy-1 attenuates TNF-Alpha-Activated gene expression in mouse embryonic fibroblasts via Src family kinase. PLos One 5, e11662, doi: 10.1371/journal.pone.0011662 (2010
70. Waldvogel, H. J., Curtis, M. A., Baer, K., Rees, M. I., & Faull, R. L. Immunohistochemical staining of post-mortem adult human brain sections. Nat Protoc 1, 2719-2732, doi: nprot.2006.354 [pii] 10.1038/nprot.2006.354 (2006
71. Gibbons, H., Sato, T. A., & Dragunow, M. Hypothermia suppresses inducible nitric oxide synthase and stimulates cyclooxygenase-2 in ipopolysaccharide stimulated BV-2 cells. Brain Res Mol Brain Res 110, 63-75, doi: S0169328X02005855 [pii] (2003
72. Livak, K. J., & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408, doi: 10.1006/meth.2001.1262 S1046-2023(01)91262-9 [pii] (2001
73. Burkert, K., Moodley, K., Angel, C. E., Brooks, A., & Graham, E. S. Detailed analysis of inflammatory and neuromodulatory cytokine secretion from human NT2 astrocytes using multiplex bead array. Neurochem Int 60, 573-580, doi: S0197-0186(11)00321-4 [pii] 10.1016/j.neuint.2011.09.002 (2012