Peripheral nerve pericytes modify the blood-nerve barrier function and tight junctional molecules through the secretion of various soluble factors

Journal of Cellular Physiology

Volumn 226, Issue 1, 2011, Pages 255-266

  Shimizu, Fumitaka ^a   Sano, Yasuteru ^a   Abe, Masa aki ^a   Maeda, Toshihiko ^a   Ohtsuki, Sumio ^b   Terasaki, Tetsuya ^b   Kanda, Takashi ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BASIC FIBROBLAST GROWTH FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CD31 ANTIGEN; CLAUDIN 5; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INULIN; NERVE GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN; PROTEIN NG2; RETROVIRUS VECTOR; TELOMERASE; TSA58; UNCLASSIFIED DRUG; VIRUS ANTIGEN; VON WILLEBRAND FACTOR;

ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD NERVE BARRIER; BRAIN; ENDOTHELIUM CELL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INULIN CLEARANCE; NERVE FIBER REGENERATION; NERVE FUNCTION; PERICYTE; PERIPHERAL NERVE; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN SECRETION; RETROVIRUS; SIMIAN VIRUS 40; UPREGULATION;

BIOLOGICAL MARKERS; BLOOD-BRAIN BARRIER; BLOOD-NERVE BARRIER; BRAIN; CELL CULTURE TECHNIQUES; CELL LINE; ELECTROPHYSIOLOGICAL PHENOMENA; GENE EXPRESSION REGULATION; HUMANS; MEMBRANE PROTEINS; NERVE GROWTH FACTORS; PERICYTES; PERIPHERAL NERVES; TIGHT JUNCTIONS;

EID: 78049231404     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22337     Document Type: Article

References (51)

1. Abbott NJ, Rönnbäck L, Hansson E. 2006. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7: 41-53.
2. Argaw AT, Gurfein BT, Zhang Y, Zameer A, John GR. 2009. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci USA 106: 1977-1982.
3. Armulik A, Abramsson A, Betsholtz C. 2005. Endothelial/pericyte interactions. Circ Res 97: 512-523.
4. Bäckman CM, Shan L, Zhang YJ, Hoffer BJ, Leonard S, Troncoso JC, Vonsatel P, Tomac AC. 2006. Gene expression patterns for GDNF and its receptors in the human putamen affected by Parkinson's disease: A real-time PCR study. Mol Cell Endocrinol 27: 160-166.
5. Basciani S, Mariani S, Arizzi M, Ulisse S, Rucci N, Jannini EA, Della Rocca C, Manicone A, Carani C, Spera G, Gnessi L. 2002. Expression of platelet-derived growth factor-A (PDGF-A), PDGF-B, and PDGF receptor-alpha and -beta during human testicular development and disease. J Clin Endocrinol Metab 87: 2310-2319.
6. Bendfeldt K, Radojevic V, Kapfhammer J, Nitsch C. 2007. Basic fibroblast growth factor modulates density of blood vessels and preserves tight junctions in organotypic cortical cultures of mice: A new in vitro model of the blood-brain barrier. J Neurosci 27: 3260-3267.
7. Boyle K, Azari MF, Cheema SS, Petratos S. 2005. TNF-alpha mediates Schwann cell death by upregulating p75NTR expression without sustained activation of NF kappaB. Neurobiol Dis 20: 412-427.
8. Bronzetti E, Artico M, Pompili E, Felici LM, Stringaro A, Bosco S, Magliulo G, Colone M, Arancia G, Vitale M, Fumagalli L. 2006. Neurotrophins and neurotransmitters in human palatine tonsils: An immunohistochemical and RT-PCR analysis. Int J Mol Med 18: 49-58.
9. Brown EB, Campbell RB, Tsuzuki Y, Xu L, Carmeliet P, Fukumura D, Jain RK. 2001. In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy. Nat Med 7: 864-868.
10. Capetandes A, Gerritsen ME. 1990. Simplified methods for consistent and selective culture of bovine retinal endothelial cells and pericytes. Invest Ophthalmol Vis Sci 31: 1738-1744.
11. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, Ryan TE, Bruno J, Radziejewski C, Maisonpierre PC, Yancopoulos GD. 1996. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 27: 1161-1169.
12. Deng H, Yang X, Jin T, Wu J, Hu LS, Chang M, Sun XJ, Adem A, Winblad B, Zhu J. 2008. The role of IL-12 and TNF-alpha in AIDP and AMAN. Eur J Neurol 15: 1100-1105.
13. Fuchs S, Hermanns MI, Kirkpatrick CJ. 2006. Retention of a differentiated endothelial phenotype by outgrowth endothelial cells isolated from human peripheral blood and expanded in long-term cultures. Cell Tissue Res 326: 79-92.
14. Ghassemifar MR, Eckert JJ, Houghton FD, Picton HM, Leese HJ, Fleming TP. 2003. Gene expression regulating epithelial intercellular junction biogenesis during human blastocyst development in vitro. Mol Hum Reprod 9: 245-252.
15. Giannini C, Dyck PJ. 1995. Basement membrane reduplication and pericyte degeneration precede development of diabetic polyneuropathy and are associated with its severity. Ann Neurol 37: 498-504.
16. Hammes HP. 2005. Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res 37: 39-43.
17. Hellstrom M, Gerhardt H, Kalen M, Li X, Eriksson U, Wolburg H, Betsholtz C. 2001. Lack of pericyte leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 30: 543-553.
18. Hirschi KK, Burt JM, Hirschi KD, Dai C. 2003. Gap junction communication mediates transforming growth factor-beta activation and endothelial-induced mural cell differentiation. Circ Res 93: 429-437.
19. Honda M, Nakagawa S, Hayashi K, Kitagawa N, Tsutsumi K, Nagata I, Niwa M. 2006. Adrenomedullin improves the blood-brain barrier function through the expression of claudin-5. Cell Mol Neurobiol 26: 109-118.
20. Hori S, Ohtsuki S, Hosoya K, Nakashima E, Terasaki T. 2004. A pericyte-derived angiopoietin-1 multimeric complex induces occludin gene expression in brain capillary endothelial cells through Tie-2 activation in vitro. J Neurochem 89: 503-513.
21. Hosoya KI, Takashima T, Tetsuka K, Nagura T, Ohtsuki S, Takanaga H, Ueda M, Yanai N, Obinata M, Terasaki T. 2000. mRNA expression and transport characterization of conditionally immortalized rat brain capillary endothelial cell lines; a new in vitro BBB model for drug targeting. J Drug Target 8: 357-370.
22. Huang YQ, Li JJ, Karpatkin S. 2000. Identification of a family of alternatively spliced mRNA species of angiopoietin-1. Blood 15: 1993-1999.
23. Kanda T, Yoshino H, Ariga T, Yamawaki M, Yu RK. 1994. Glycosphinogolipid antigens in cultured microvascular bovine brain endothelial cells: Sulfoglucuronosyl paragloboside as a target of monoclonal IgM in demyelinative neuropathy. J Cell Biol 126: 235-246.
24. Kanda T, Iwasaki T, Yamawaki M, Ikeda K. 1997. Isolation and culture of bovine endothelial cells of endoneurial origin. J Neurosci Res 15: 769-777.
25. Kanda T, Yamawaki M, Iwasaki T, Mizusawa H. 2000. Glycosphingolipid antibodies and blood-nerve barrier in autoimmune demyelinative neuropathy. Neurology 54: 1459-1464.
26. Kanda T, Numata Y, Mizusawa H. 2004. Chronic inflammatory demyelinating polyneuropathy: Decreased claudin-5 and relocated ZO-1. J Neurol Neurosurg Psychiatry 75: 765-769.
27. Kim JH, Kim JH, Park JA, Lee SW, Kim WJ, Yu YS, Kim KW. 2006. Blood-neural barrier: Intercellular communication at glio-vascular interface. J Biochem Mol Biol 39: 339-345.
28. Kondo T, Hosoya K, Hori S, Tomi M, Ohtsuki S, Takanaga H, Nakashima E, Iizasa H, Asashima T, Ueda M, Obinata M, Terasaki T. 2003. Establishment of conditionally immortalized rat retinal pericyte cell lines (TR-rPCT) and their application in a co-culture system using retinal capillary endothelial cell line (TR-iBRB2). Cell Struct Funct 28: 145-153.
29. Lach B, Rippstein P, Atack D, Afar DE, Gregor A. 1993. Immunoelectron microscopic localization of monoclonal IgM antibodies in gammopathy associated with peripheral demyelinative neuropathy. Acta Neuropathol 85: 298-307.
30. Lindahl P, Johansson BR, Leveen P, Betsholtz C. 1997. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277: 242-245.
31. Mizuta I, Ohta M, Ohta K, Nishimura M, Mizuta E, Kuno S. 2001. Riluzole stimulates nerve growth factor, brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor synthesis in cultured mouse astrocytes. Neurosci Lett 310: 117-120.
32. Nehls V, Drenckhahn D. 1991. Heterogeneity of microvascular pericytes for smooth muscle type alpha-actin. J Cell Biol 113: 147-154.
33. Niimi H. 2003. Cerebral angiogenesis induced by growth factors: Intravital microscopic studies using models. Clin Hemorheol Microcirc 29: 149-156.
34. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, Furuse M, Tsukita S. 2003. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 161: 653-660.
35. Ohtsuki S, Sato S, Yamaguchi H, Kamoi M, Asashima T, Terasaki T. 2007. Exogenous expression of claudin-5 induces barrier properties in cultured rat brain capillary endothelial cells. J Cell Physiol 210: 81-86.
36. Ozerdem U, Grako KA, Dahlin-Huppe K, Monosov E, Stallcup WB. 2001. NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev Dyn 222: 218-227.
37. Poduslo JF, Curran GL, Berg CT. 1994. Macromolecular permeability across the blood-nerve and blood-brain barriers. Proc Natl Acad Sci USA 91: 5705-5709.
38. Radhakrishnan VV, Sumi MG, Reuben S, Mathai A, Nair MD. 2004. Serum tumour necrosis factor-alpha and soluble tumour necrosis factor receptors levels in patients with Guillain-Barre syndrome. Acta Neurol Scand 109: 71-74.
39. Reinmuth N, Liu W, Jung YD, Ahmad SA, Shaheen RM, Fan F, Bucana CD, McMahon G, Gallick GE, Ellis LM. 2001. Induction of VEGF in perivascular cells defines a potential paracrine mechanism for endothelial cell survival. FASEB J 15: 1239-1241.
40. Said HM, Hagemann C, Staab A, Stojic J, Kühnel S, Vince GH, Flentje M, Roosen K, Vordermark D. 2007. Expression patterns of the hypoxia-related genes osteopontin, CA9, erythropoietin, VEGF and HIF-1alpha in human glioma in vitro and in vivo. Radiother Oncol 83: 398-405.
41. Sano Y, Shimizu F, Nakayama H, Abe M, Maeda T, Ohtsuki S, Terasaki T, Obinata M, Ueda M, Takahashi R, Kanda T. 2007. Endothelial cells constituting blood-nerve barrier have highly specialized characteristics as barrier-forming cells. Cell Struct Funct 32: 139-147.
42. Sano Y, Shimizu F, Abe M, Maeda T, Kashiwamura Y, Ohtsuki S, Terasaki T, Obinata M, Kajiwara K, Fujii M, Suzuki M, Kanda T. 2010. Establishment of a new conditionally immortalized human brain microvascular endothelial cell line retaining an in vivo blood-brain barrier function. J Cell Physiol 10 (in press).
43. Sato Y, Rifkin DB. 1989. Inhibition of endothelial cell movement by pericytes and smooth muscle cells: Activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture. J Cell Biol 109: 309-315.
44. Shepro D, Morel NM. 1993. Pericyte physiology. FASEB J 7: 1031-1038.
45. Shimizu F, Sano Y, Maeda T, Abe MA, Nakayama H, Takahashi R, Ueda M, Ohtsuki S, Terasaki T, Obinata M, Kanda T. 2008. Peripheral nerve pericytes originating from the blood-nerve barrier expresses tight junctional molecules and transporters as barrier-forming cells. J Cell Physiol 217: 388-399.
46. Soufla G, Sifakis S, Baritaki S, Zafiropoulos A, Koumantakis E, Spandidos DA. 2005. VEGF, FGF2, TGFB1 and TGFBR1 mRNA expression levels correlate with the malignant transformation of the uterine cervix. Cancer Lett 18: 105-118.
47. Varley CL, Garthwaite MA, Cross W, Hinley J, Trejdosiewicz LK, Southgate J. 2006. PPARgamma-regulated tight junction development during human urothelial cytodifferentiation. J Cell Physiol 208: 407-417.
48. Wang Y, Chang CF, Morales M, Chiang YH, Hoffer J. 2002. Protective effects of glial cell line-derived neurotrophic factor in ischemic brain injury. Ann N Y Acad Sci 962: 423-437.
49. Weksler BB, Subileau EA, Perrière N, Charneau P, Holloway K, Leveque M, Tricoire-Leignel H, Nicotra A, Bourdoulous S, Turowski P, Male DK, Roux F, Greenwood J, Romero IA, Couraud PO. 2005. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 19: 1872-1874.
50. Yang X, Jin T, Press R, Quezada HC, Fredrikson S, Zhu J. 2008. The expression of TNF-alpha receptors 1 and 2 on peripheral blood mononuclear cells in chronic inflammatory demyelinating polyneuropathy. J Neuroimmunol 200: 129-132.
51. Zhang ZL, Liu ZS, Sun Q. 2006. Expression of angiopoietins, Tie2 and vascular endothelial growth factor in angiogenesis and progression of hepatocellular carcinoma. World J Gastroenterol 12: 4241-4245.