Isolation and functional characterization of pericytes derived from hamster skeletal muscle

Acta Physiologica

Volumn 201, Issue 4, 2011, Pages 413-426

  Mogensen, C ^a,b   Bergner, B ^a   Wallner, S ^a   Ritter, A ^a   d'Avis, S ^a   Ninichuk, V ^a   Kameritsch, P ^a   Gloe, T ^a,c   Nagel, W ^a   Pohl, U ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Cell culture; Interleukin 8; Kv1.5 channel; Pericyte; Skeletal muscle

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CONNEXIN 43; INTERLEUKIN 8; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; POTASSIUM CHANNEL KV1.5; PROTEOGLYCAN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL ISOLATION; CELL MEMBRANE POTENTIAL; CELL STRUCTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; GAP JUNCTION; HAMSTER; HUMAN; HUMAN CELL; HYPERPOLARIZATION; LEG MUSCLE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; SKELETAL MUSCLE; THIGH; UMBILICAL VEIN;

ANIMALS; BIOLOGICAL MARKERS; CELL SEPARATION; CELLS, CULTURED; CONNEXIN 43; CRICETINAE; GAP JUNCTIONS; HELA CELLS; HUMANS; IMMUNOMAGNETIC SEPARATION; INTERLEUKIN-8; KV1.5 POTASSIUM CHANNEL; MEMBRANE POTENTIALS; MESOCRICETUS; MUSCLE, SKELETAL; PATCH-CLAMP TECHNIQUES; PERICYTES;

EID: 79952526457     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2010.02206.x     Document Type: Article

References (74)

1. Allt, G. & Lawrenson, J.G. 2001. Pericytes: cell biology and pathology. Cells Tissues Organs 169, 1-11.
2. Andreeva, E.R., Pugach, I.M., Gordon, D. & Orekhov, A.N. 1998. Continuous subendothelial network formed by pericyte-like cells in human vascular bed. Tissue Cell 30, 127-135.
3. Armulik, A., Abramsson, A. & Betsholtz, C. 2005. Endothelial/pericyte interactions. Circ Res 97, 512-523.
4. Baluk, P., Hashizume, H. & McDonald, D.M. 2005. Cellular abnormalities of blood vessels as targets in cancer. Curr Opin Genet Dev 15, 102-111.
5. Bandopadhyay, R., Orte, C., Lawrenson, J.G., Reid, A.R., De Silva, S. & Allt, G. 2001. Contractile proteins in pericytes at the blood-brain and blood-retinal barriers. J Neurocytol 30, 35-44.
6. von Beckerath, N., Nees, S., Neumann, F.J., Krebs, B., Juchem, G. & Schomig, A. 2000. An inward rectifier and a voltage-dependent K+ current in single, cultured pericytes from bovine heart. Cardiovasc Res 46, 569-578.
7. Beltramo, E., Buttiglieri, S., Pomero, F., Allione, A., D'Alu, F., Ponte, E. & Porta, M. 2003. A study of capillary pericyte viability on extracellular matrix produced by endothelial cells in high glucose. Diabetologia 46, 409-415.
8. Berg, B.R., Cohen, K.D. & Sarelius, I.H. 1997. Direct coupling between blood flow and metabolism at the capillary level in striated muscle. Am J Physiol 272, H2693-H2700.
9. Bergers, G. & Song, S. 2005. The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 7, 452-464.
10. Berrone, E., Beltramo, E., Buttiglieri, S., Tarallo, S., Rosso, A., Hammes, H.P. & Porta, M. 2009. Establishment and characterization of a human retinal pericyte line: a novel tool for the study of diabetic retinopathy. Int J Mol Med 23, 373-378.
11. Bondjers, C., He, L., Takemoto, M., Norlin, J., Asker, N., Hellstrom, M., Lindahl, P. & Betsholtz, C. 2006. Microarray analysis of blood microvessels from PDGF-B and PDGF-Rbeta mutant mice identifies novel markers for brain pericytes. FASEB J 20, 1703-1705.
12. Brauner, T., Hulser, D.F. & Strasser, R.J. 1984. Comparative measurements of membrane potentials with microelectrodes and voltage-sensitive dyes. Biochim Biophys Acta 771, 208-216.
13. Brekke, J.F., Jackson, W.F. & Segal, S.S. 2006. Arteriolar smooth muscle Ca2+ dynamics during blood flow control in hamster cheek pouch. J Appl Physiol 101, 307-315.
14. Bryan, B.A. & D'Amore, P.A. 2008. Pericyte isolation and use in endothelial/pericyte coculture models. Methods: Enzymol 443, 315-331.
15. Capetandes, A. & Gerritsen, M.E. 1990. Simplified methods for consistent and selective culture of bovine retinal endothelial cells and pericytes. Invest Ophthalmol Vis Sci 31, 1738-1744.
16. Cheong, A., Dedman, A.M., Xu, S.Z. & Beech, D.J. 2001. K(V)alpha1 channels in murine arterioles: differential cellular expression and regulation of diameter. Am J Physiol Heart Circ Physiol 281, H1057-H1065.
17. Dellavalle, A., Sampaolesi, M., Tonlorenzi, R., Tagliafico, E., Sacchetti, B., Perani, L., Innocenzi, A., Galvez, B.G., Messina, G., Morosetti, R. et al. 2007. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9, 255-267.
18. Dente, C.J., Steffes, C.P., Speyer, C. & Tyburski, J.G. 2001. Pericytes augment the capillary barrier in in vitro cocultures. J Surg Res 97, 85-91.
19. Dora, K.A., Xia, J. & Duling, B.R. 2003. Endothelial cell signaling during conducted vasomotor responses. Am J Physiol Heart Circ Physiol 285, H119-H126.
20. Egginton, S., Hudlicka, O., Brown, M.D., Graciotti, L. & Granata, A.L. 1996. In vivo pericyte-endothelial cell interaction during angiogenesis in adult cardiac and skeletal muscle. Microvasc Res 51, 213-228.
21. Epps, D.E., Wolfe, M.L. & Groppi, V. 1994. Characterization of the steady-state and dynamic fluorescence properties of the potential-sensitive dye bis-(1, 3-dibutylbarbituric acid)trimethine oxonol (Dibac4(3)) in model systems and cells. Chem Phys Lipids 69, 137-150.
22. Farrington-Rock, C., Crofts, N.J., Doherty, M.J., Ashton, B.A., Griffin-Jones, C. & Canfield, A.E. 2004. Chondrogenic and adipogenic potential of microvascular pericytes. Circulation 110, 2226-2232.
23. Farrugia, G., Rae, J.L., Sarr, M.G. & Szurszewski, J.H. 1993. Potassium current in circular smooth muscle of human jejunum activated by fenamates. Am J Physiol 265, G873-G879.
24. Frydelund-Larsen, L., Penkowa, M., Akerstrom, T., Zankari, A., Nielsen, S. & Pedersen, B.K. 2007. Exercise induces interleukin-8 receptor (CXCR2) expression in human skeletal muscle. Exp Physiol 92, 233-240.
25. Fujimoto, K. 1995. Pericyte-endothelial gap junctions in developing rat cerebral capillaries: a fine structural study. Anat Rec 242, 562-565.
26. Giatromanolaki, A., Sivridis, E., Maltezos, E. & Koukourakis, M.I. 2002. Down-regulation of intestinal-type alkaline phosphatase in the tumor vasculature and stroma provides a strong basis for explaining amifostine selectivity. Semin Oncol 29, 14-21.
27. Gitlin, J.D. & D'Amore, P.A. 1983. Culture of retinal capillary cells using selective growth media. Microvasc Res 26, 74-80.
28. Griffith, T.M., Chaytor, A.T. & Edwards, D.H. 2004. The obligatory link: role of gap junctional communication in endothelium-dependent smooth muscle hyperpolarization. Pharmacol Res 49, 551-564.
29. Helmbold, P., Nayak, R.C., Marsch, W.C. & Herman, I.M. 2001a. Isolation and in vitro characterization of human dermal microvascular pericytes. Microvasc Res 61, 160-165.
30. Helmbold, P., Wohlrab, J., Marsch, W.C. & Nayak, R.C. 2001b. Human dermal pericytes express 3G5 ganglioside--a new approach for microvessel histology in the skin. J Cutan Pathol 28, 206-210.
31. Hirschi, K.K. & D'Amore, P.A. 1996. Pericytes in the microvasculature. Cardiovasc Res 32, 687-698.
32. Hirschi, K.K., Burt, J.M., Hirschi, K.D. & Dai, C. 2003. Gap junction communication mediates transforming growth factor-beta activation and endothelial-induced mural cell differentiation. Circ Res 93, 429-437.
33. Hoepfl, B., Rodenwaldt, B., Pohl, U. & De Wit, C. 2002. EDHF, but not NO or prostaglandins, is critical to evoke a conducted dilation upon ACh in hamster arterioles. Am J Physiol Heart Circ Physiol 283, H996-H1004.
34. Hoffmann, A., Gloe, T., Pohl, U. & Zahler, S. 2003. Nitric oxide enhances de novo formation of endothelial gap junctions. Cardiovasc Res 60, 421-430.
35. Hughes, S. & Chan-Ling, T. 2004. Characterization of smooth muscle cell and pericyte differentiation in the rat retina in vivo. Invest Ophthalmol Vis Sci 45, 2795-2806.
36. Jackson, W.F. 2005. Potassium channels in the peripheral microcirculation. Microcirculation 12, 113-127.
37. Kameritsch, P., Khandoga, N., Nagel, W., Hundhausen, C., Lidington, D. & Pohl, U. 2005. Nitric oxide specifically reduces the permeability of Cx37-containing gap junctions to small molecules. J Cell Physiol 203, 233-242.
38. Krötz, F., Engelbrecht, B., Buerkle, M.A., Bassermann, F., Bridell, H., Gloe, T., Duyster, J., Pohl, U. & Sohn, H.Y. 2005. The tyrosine phosphatase, SHP-1, is a negative regulator of endothelial superoxide formation. J Am Coll Cardiol 45, 1700-1706.
39. Lamagna, C. & Bergers, G. 2006. The bone marrow constitutes a reservoir of pericyte progenitors. J Leukoc Biol 80, 677-681.
40. Larson, D.M., Carson, M.P. & Haudenschild, C.C. 1987. Junctional transfer of small molecules in cultured bovine brain microvascular endothelial cells and pericytes. Microvasc Res 34, 184-199.
41. Li, A.F., Sato, T., Haimovici, R., Okamoto, T. & Roy, S. 2003. High glucose alters connexin 43 expression and gap junction intercellular communication activity in retinal pericytes. Invest Ophthalmol Vis Sci 44, 5376-5382.
42. Liu, Y., Wilkinson, F.L., Kirton, J.P., Jeziorska, M., Iizasa, H., Sai, Y., Nakashima, E., Heagerty, A.M., Canfield, A.E. & Alexander, M.Y. 2007. Hepatocyte growth factor and c-Met expression in pericytes: implications for atherosclerotic plaque development. J Pathol 212, 12-19.
43. Lückhoff, A. & Busse, R. 1990. Calcium influx into endothelial cells and formation of endothelium-derived relaxing factor is controlled by the membrane potential. Pflugers Arch 416, 305-311.
44. Lunkenheimer, P.P. & Merker, H.J. 1976. Distribution of alkaline phosphatase in the microcirculatory pathways of the coronary system. Acta Histochem 57, 14-19.
45. McMurdo, L., Stephenson, A.H., Baldassare, J.J., Sprague, R.S. & Lonigro, A.J. 1998. Biosynthesis of sulfidopeptide leukotrienes via the transfer of leukotriene A4 from polymorphonuclear cells to bovine retinal pericytes. J Pharmacol Exp Ther 285, 1255-1259.
46. Murfee, W.L., Skalak, T.C. & Peirce, S.M. 2005. Differential arterial/venous expression of NG2 proteoglycan in perivascular cells along microvessels: identifying a venule-specific phenotype. Microcirculation 12, 151-160.
47. Murfee, W.L., Rehorn, M.R., Peirce, S.M. & Skalak, T.C. 2006. Perivascular cells along venules upregulate NG2 expression during microvascular remodeling. Microcirculation 13, 261-273.
48. Murrant, C.L. & Sarelius, I.H. 2002. Multiple dilator pathways in skeletal muscle contraction-induced arteriolar dilations. Am J Physiol Regul Integr Comp Physiol 282, R969-R978.
49. Nayak, R.C., Berman, A.B., George, K.L., Eisenbarth, G.S. & King, G.L. 1988. A monoclonal antibody (3G5)-defined ganglioside antigen is expressed on the cell surface of microvascular pericytes. J Exp Med 167, 1003-1015.
50. Nehls, V., Schuchardt, E. & Drenckhahn, D. 1994. The effect of fibroblasts, vascular smooth muscle cells, and pericytes on sprout formation of endothelial cells in a fibrin gel angiogenesis system. Microvasc Res 48, 349-363.
51. Newcomb, P.M. & Herman, I.M. 1993. Pericyte growth and contractile phenotype: modulation by endothelial-synthesized matrix and comparison with aortic smooth muscle. J Cell Physiol 155, 385-393.
52. Orlidge, A. & D'Amore, P.A. 1987. Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J Cell Biol 105, 1455-1462.
53. Ozerdem, U. & Stallcup, W.B. 2003. Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 6, 241-249.
54. Pomero, F., Allione, A., Beltramo, E., Buttiglieri, S., D'Alu, F., Ponte, E., Lacaria, A. & Porta, M. 2003. Effects of protein kinase C inhibition and activation on proliferation and apoptosis of bovine retinal pericytes. Diabetologia 46, 416-419.
55. + channels in cultured bovine retinal pericytes: effects of beta-adrenergic stimulation. J Cardiovasc Pharmacol 42, 379-388.
56. Romanul, F.C. & Bannister, R.G. 1962. Localized areas of high alkaline phosphatase activity in the terminal arterial tree. J Cell Biol 15, 73-84.
57. Sakagami, K., Wu, D.M. & Puro, D.G. 1999. Physiology of rat retinal pericytes: modulation of ion channel activity by serum-derived molecules. J Physiol 521, 637-650.
58. Sandow, S.L., Looft-Wilson, R., Doran, B., Grayson, T.H., Segal, S.S. & Hill, C.E. 2003. Expression of homocellular and heterocellular gap junctions in hamster arterioles and feed arteries. Cardiovasc Res 60, 643-653.
59. Segal, S.S. 1991. Microvascular recruitment in hamster striated muscle: role for conducted vasodilation. Am J Physiol 261, H181-H189.
60. Shepro, D. & Morel, N.M. 1993. Pericyte physiology. FASEB J 7, 1031-1038.
61. Shih, S.C., Ju, M., Liu, N., Mo, J.R., Ney, J.J. & Smith, L.E. 2003. Transforming growth factor beta1 induction of vascular endothelial growth factor receptor 1: mechanism of pericyte-induced vascular survival in vivo. Proc Natl Acad Sci U S A 100, 15859-15864.
62. Siegl, D., Koeppen, M., Wolfle, S.E., Pohl, U. & de Wit, C. 2005. Myoendothelial coupling is not prominent in arterioles within the mouse cremaster microcirculation in vivo. Circ Res 97, 781-788.
63. Song, S., Ewald, A.J., Stallcup, W., Werb, Z. & Bergers, G. 2005. PDGFRbeta+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol 7, 870-879.
64. Stallcup, W.B. 2002. The NG2 proteoglycan: past insights and future prospects. J Neurocytol 31, 423-435.
65. Stitt, A.W., Hughes, S.J., Canning, P., Lynch, O., Cox, O., Frizzell, N., Thorpe, S.R., Cotter, T.G., Curtis, T.M. & Gardiner, T.A. 2004. Substrates modified by advanced glycation end-products cause dysfunction and death in retinal pericytes by reducing survival signals mediated by platelet-derived growth factor. Diabetologia 47, 1735-1746.
66. Sundberg, C., Kowanetz, M., Brown, L.F., Detmar, M. & Dvorak, H.F. 2002. Stable expression of angiopoietin-1 and other markers by cultured pericytes: phenotypic similarities to a subpopulation of cells in maturing vessels during later stages of angiogenesis in vivo. Lab Invest 82, 387-401.
67. Swinscoe, J.C. & Carlson, E.C. 1992. Capillary endothelial cells secrete a heparin-binding mitogen for pericytes. J Cell Sci 103, 453-461.
68. Tyml, K., Song, H., Munoz, P. & Ouellette, Y. 1997. Evidence for K+ channels involvement in capillary sensing and for bidirectionality in capillary communication. Microvasc Res 53, 245-253.
69. Veliz, L.P., Gonzalez, F.G., Duling, B.R., Saez, J.C. & Boric, M.P. 2008. Functional role of gap junctions in cytokine-induced leukocyte adhesion to endothelium in vivo. Am J Physiol Heart Circ Physiol 295, H1056-H1066.
70. de Wit, C. 2010. Different pathways with distinct properties conduct dilations in the microcirculation in vivo. Cardiovasc Res 85, 604-613.
71. de Wit, C. & Griffith, T.M. 2010. Connexins and gap junctions in the EDHF phenomenon and conducted vasomotor responses. Pflugers Arch 459, 897-914.
72. de Wit, C., Roos, F., Bolz, S.S., Kirchhoff, S., Kruger, O., Willecke, K. & Pohl, U. 2000. Impaired conduction of vasodilation along arterioles in connexin40-deficient mice. Circ Res 86, 649-655.
73. Yamagishi, S., Inagaki, Y., Amano, S., Okamoto, T. & Takeuchi, M. 2002. Up-regulation of vascular endothelial growth factor and down-regulation of pigment epithelium-derived factor messenger ribonucleic acid levels in leptin-exposed cultured retinal pericytes. Int J Tissue React 24, 137-142.
74. Yeh, H.I., Rothery, S., Dupont, E., Coppen, S.R. & Severs, N.J. 1998. Individual gap junction plaques contain multiple connexins in arterial endothelium. Circ Res 83, 1248-1263.