Isolation, bulk cultivation, and characterization of coronary microvascular pericytes: The second most frequent myocardial cell type in vitro

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 1, 2012, Pages

  Nees, Stephan ^a   Weiss, Dominik R ^b   Senfti, Anton ^a   Knott, Maria ^a   Förch, Stefan ^a   Schnurr, Maximilian ^a   Weyrich, Peter ^a   Juchem, Gerd ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Angiogenesis; Coronary system; Endothelial cells; Inflammation; Tissue factor

Indexed keywords

ALPHA ACTIN; BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 10A; CALCEIN; NITROGEN; PROTHROMBIN; THROMBOPLASTIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BLOOD FLOW; CATTLE; CELL COMMUNICATION; CELL CULTURE; CELL GROWTH; CELL ISOLATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CORONARY BLOOD VESSEL; DENSITY GRADIENT CENTRIFUGATION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; GUINEA PIG; HEART MUSCLE; HEART MUSCLE CELL; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PURIFICATION; RABBIT; RAT; SMOOTH MUSCLE FIBER; SWINE; VASCULAR ENDOTHELIUM;

ANIMALS; BLOOD COAGULATION; CATTLE; CELL COMMUNICATION; CELL PROLIFERATION; CELL SEPARATION; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; CORONARY VESSELS; CRICETINAE; CRYOPRESERVATION; ENDOTHELIAL CELLS; GUINEA PIGS; HUMANS; MESOCRICETUS; MICE; MICROVESSELS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOVASCULARIZATION, PHYSIOLOGIC; PERICYTES; PHENOTYPE; RABBITS; RATS; RATS, SPRAGUE-DAWLEY; SUS SCROFA; TIME FACTORS;

EID: 84255182434     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00359.2011     Document Type: Article

References (102)

1. Adams RH, Alitalo K. Molecular regulation of angiogenesis and lym-phangiogenesis. Nat Rev Mol Cell Biol 8: 464-478, 2007.
2. Aikawa M, Libby P. The vulnerable atherosclerotic plaque: pathogen-esis and therapeutic approach. Cardiovasc Pathol 13: 125-138, 2004.
3. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res 97: 512-523, 2005.
4. Balabanov R, Beaumont T, Dore-Duffy P. Role of central nervous system microvascular pericytes in activation of antigen-primed splenic T-lymphocytes. J Neurosci Res 55: 578-587, 1999.
5. Bär T, Budi Santoso AW. Identification of pericytes in the central nervous system by silver staining of the basal lamina. Cell Tissue Res 236: 491-493, 1984.
6. Bergers G, Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 7: 452-464, 2005.
7. Bouchard BA, Shatos MA, Tracy PB. Human brain pericytes differentially regulate expression of procoagulant enzyme complexes comprising the extrinsic pathway of blood coagulation. Arterioscler Thromb Vasc Biol 17: 1-9, 1997.
8. Boulanger CM, Dignat-George F. Microparticles: an introduction. Arterioscler Thromb Vasc Biol 31: 2-3, 2011.
9. Carmeliet P. Angiogenesis in health and disease. Nat Med 9: 653-660, 2003.
10. Corselli M, Chen CW, Crisan M, Lazzari L, Peault B. Perivascular ancestors of adult multipotent stem cells. Arterioscler Thromb Vasc Biol 30: 1104-1109, 2010.
11. Crane GJ, Neild TO, Segal SS. Contribution of active membrane processes to conducted hyperpolarization in arterioles of hamster cheek pouch. Microcirculation 11: 425-433, 2004.
12. Cui L, Ju Y, Ding L, Trejo-Morales M, Olfert IM. Arteriolar and venular capillary distribution in skeletal muscles of old rats. J Gerontol A Biol Sci Med Sci 63: 928-935, 2008.
13. Czirok A, Zamir EA, Szabo A, Little CD. Multicellular sprouting during vasculogenesis. Curr Top Dev Biol 81: 269-289, 2008.
14. Davidoff MS, Middendorff R, Muller D, Holstein AF. The neuroen-docrine Leydig cells and their stem cell progenitors, the pericytes. Adv Anat Embryol Cell Biol 205: 1-107, 2009.
15. De Smet F, Segura I, De Bock K, Hohensinner PJ, Carmeliet P. Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler Thromb Vasc Biol 29: 639-649, 2009.
16. de Wit C, Boettcher M, Schmidt VJ. Signaling across myoendothelial gap junctions-fact or fiction? Cell Commun Adhes 15: 231-245, 2008.
17. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R, Li S, Belicchi M, Peretti G, Chamberlain JS, Wright WE, Torrente Y, Ferrari S, Bianco P, Cossu G. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9: 255- 267, 2007.
18. Dente CJ, Steffes CP, Speyer C, Tyburski JG. Pericytes augment the capillary barrier in in vitro cocultures. J Surg Res 97: 85-91, 2001.
19. Diaz-Flores L, Gutierrez R, Madrid JF, Varela H, Valladares F, Acosta E, Martin-Vasallo P, Diaz-Flores L. Pericytes morphofunc-tion, interactions and pathology in a quiescent and activated mesenchy-mal cell niche. Histol Histopathol 24: 909-969, 2009.
20. Diaz-Flores L, Gutierrez R, Varela H. Angiogenesis: an update. Histol Histopathol 9: 807-843, 1994.
21. Dignat-George F, Boulanger CM. The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 31: 27-33, 2011.
22. Dore-Duffy P. Isolation and characterization of cerebral microvascular pericytes. Methods Mol Med 89: 375-382, 2003.
23. Dore-Duffy P. Pericytes: pluripotent cells of the blood brain barrier. Curr Pharm Des 14: 1581-1593, 2008.
24. Eble JA, Niland S. The extracellular matrix of blood vessels. Curr Pharm Des 15: 1385-1400, 2009.
25. Eichmann A, Le Noble F, Autiero M, Carmeliet P. Guidance of vascular and neural network formation. Curr Opin Neurobiol 15: 108-115, 2005.
26. Emerson GG, Neild TO, Segal SS. Conduction of hyperpolarization along hamster feed arteries: augmentation by acetylcholine. Am J Physiol Heart Circ Physiol 283: H102-H109, 2002.
27. Fernandez-Klett F, Offenhauser N, Dirnagl U, Priller J, Lindauer U. Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain. Proc Natl Acad Sci USA 107: 22290-22295, 2010.
28. Figueroa XF, Chen CC, Campbell KP, Damon DN, Day KH, Ramos S, Duling BR. Are voltage-dependent ion channels involved in the endothelial cell control of vasomotor tone? Am J Physiol Heart Circ Physiol 293: H1371-H1383, 2007.
29. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161: 1163-1177, 2003.
30. Giatromanolaki A, Sivridis E, Maltezos E, Koukourakis MI. Down-regulation of intestinal-type alkaline phosphatase in the tumor vascula-ture and stroma provides a strong basis for explaining amifostine selectivity. Semin Oncol 29: 14-21, 2002.
31. Haas TL, Duling BR. Morphology favors an endothelial cell pathway for longitudinal conduction within arterioles. Microvasc Res 53: 113-120, 1997.
32. Hammersen F, Hammersen E. Some structural aspects of precapillary vessels. J Cardiovasc Pharmacol 6, Suppl 2: S289-S303, 1984.
33. Hammes HP. Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res 37, Suppl 1: 39-43, 2005.
34. Hellberg C, Ostman A, Heldin CH. PDGF and vessel maturation. Recent Results Cancer Res 180: 103-114, 2010.
35. Helmbold P, Nayak RC, Marsch WC, Herman IM. Isolation and in vitro characterization of human dermal microvascular pericytes. Micro-vasc Res 61: 160-165, 2001.
36. Higuchi K, Hashizume H, Aizawa Y, Ushiki T. Scanning electron microscopic studies of the vascular smooth muscle cells and pericytes in the rat heart. Arch Histol Cytol 63: 115-126, 2000.
37. Hirschi KK, D'Amore PA. Control of angiogenesis by the pericyte: molecular mechanisms and significance. EXS 79: 419-428, 1997.
38. Hutchings H, Ortega N, Plouet J. Extracellular matrix-bound vascular endothelial growth factor promotes endothelial cell adhesion, migration, and survival through integrin ligation. FASEB J 17: 1520-1522, 2003.
39. Isakson BE, Best AK, Duling BR. Incidence of protein on actin bridges between endothelium and smooth muscle in arterioles demonstrates heterogeneous connexin expression and phosphorylation. Am J Physiol Heart Circ Physiol 294: H2898-H2904, 2008.
40. Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest 52: 2745-2756, 1973.
41. Juchem G, Weiss DR, Gansera B, Kemkes BM, Mueller-Hoecker J, Nees S. Pericytes in the macrovascular intima: possible physiological and pathogenetic impact. Am J Physiol Heart Circ Physiol 298: H754-H770, 2010.
42. Juchem G, Weiss DR, Knott M, Senftl A, Förch S, Fischlein T, Kreuzer E, Reichart B, Laufer S, Nees S. Regulation of coronary venular barrier function by blood borne inflammatory mediators and pharmacological tools: insights from novel microvascular wall models. Am J Physiol Heart Circ Physiol. Published online ahead of print November 11, 2011; doi:10.1152/ajpheart.00360.2011.
43. Kamouchi M, Ago T, Kitazono T. Brain pericytes: emerging concepts and functional roles in brain homeostasis. Cell Mol Neurobiol 2010.
44. Kang SG, Shinojima N, Hossain A, Gumin J, Yong RL, Colman H, Marini F, Andreeff M, Lang FF. Isolation and perivascular localization of mesenchymal stem cells from mouse brain. Neurosurgery 67: 711-720, 2010.
45. Karamysheva AF. Mechanisms of angiogenesis. Biochemistry (Mosc) 73: 751-762, 2008.
46. Korff T, Augustin HG. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci 112: 3249-3258, 1999.
47. Krueger M, Bechmann I. CNS pericytes: concepts, misconceptions, and a way out. Glia 58: 1-10, 2010.
48. Kutcher ME, Herman IM. The pericyte: cellular regulator of micro-vascular blood flow. Microvasc Res 77: 235-246, 2009.
49. le Noble F, Klein C, Tintu A, Pries A, Buschmann I. Neural guidance molecules, tip cells, and mechanical factors in vascular development. Cardiovasc Res 78: 232-241, 2008.
50. Li AF, Sato T, Haimovici R, Okamoto T, Roy S. High glucose alters connexin 43 expression and gap junction intercellular communication activity in retinal pericytes. Invest Ophthalmol Vis Sci 44: 5376-5382, 2003.
51. Little TL, Xia J, Duling BR. Dye tracers define differential endothelial and smooth muscle coupling patterns within the arteriolar wall. Circ Res 76: 498-504, 1995.
52. Lunkenheimer PP, Merker HJ. Distribution of alkaline phosphatase in the microcirculatory pathways of the coronary system. Acta Histochem 57: 14-19, 1976.
53. Maier CL, Shepherd BR, Yi T, Pober JS. Explant outgrowth, propagation and characterization of human pericytes. Microcirculation 17: 367-380, 2010.
54. Mall F. Die blut- und lymphwege im dünndarm des hundes. Ber Königl Sächs Ges Wiss 14: 151-189, 1888.
55. Martinez MC, Tesse A, Zobairi F, Andriantsitohaina R. Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am J Physiol Heart Circ Physiol 288: H1004-H1009, 2005.
56. Mattfeldt T, Mall G. Dipyridamole-induced capillary endothelial cell proliferation in the rat heart-a morphometric investigation. Cardiovasc Res 17: 229-237, 1983.
57. Mazanet R, Franzini-Armstrong C. Scanning electron microscopy of pericytes in rat red muscle. Microvasc Res 23: 361-369, 1982.
58. Mitra AK, Dhume AS, Agrawal DK. "Vulnerable plaques"-ticking of the time bomb. Can J Physiol Pharmacol 82: 860-871, 2004.
59. Mogensen CB, Wallner S, Ritter A, d'Avis S, Ninichuk V, Ka-meritsch P, Gloe T, Nagel W, Pohl U. Isolation and functional characterization of pericytes derived from hamster skeletal muscle. Acta Physiol (Oxf) 201: 1748-1716, 2011.
60. Morrell CN, Sun H, Swaim AM, Baldwin WM. Platelets an inflammatory force in transplantation. Am J Transplant 7: 2447-2454, 2007.
61. Morse LS, Sidikaro Y. Isolation and characterization of bovine choroidal microvessel endothelium and pericytes in culture. Curr Eye Res 9: 631-642, 1990.
62. Murakami T. A revised tannin-osmium method for non-coated scanning electron microscope specimens. Arch Histol Jpn 36: 189-193, 1974.
63. Nayak RC, Herman IM. Bovine retinal microvascular pericytes: isolation, propagation, and identification. Methods Mol Med 46: 247-263, 2001.
64. Nees S, Juchem G, Eberhorn N, Thallmair M, Forch S, Knott M, Senftl A, Fischlein T, Reichart B, Weiss DR. Wall structures of myocardial precapillary arterioles and postcapillary venules reexamined and reconstructed in vitro for studies on barrier functions. Am J Physiol Heart Circ Physiol. Published online ahead of print October 7, 2011; doi:10.1152/ajpheart.00358.2011.
65. Nehls V, Denzer K, Drenckhahn D. Pericyte involvement in capillary sprouting during angiogenesis in situ. Cell Tissue Res 270: 469-474, 1992.
66. Osterud B, Bjorklid E. Sources of tissue factor. Semin Thromb Hemost 32: 11-23, 2006.
67. Ozer K, Cilingiroglu M. Vulnerable plaque: definition, detection, treatment, and future implications. Curr Atheroscler Rep 7: 121-126, 2005.
68. Ozerdem U, Stallcup WB. Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 6: 241-249, 2003.
69. Poston RS, Gu J, Brown JM, Gammie JS, White C, Nie L, Pierson RN, Griffith BP. Endothelial injury and acquired aspirin resistance as promoters of regional thrombin formation and early vein graft failure after coronary artery bypass grafting. J Thorac Cardiovasc Surg 131: 122-130, 2006.
70. Powell T, Twist VW. A rapid technique for the isolation and purification of adult cardiac muscle cells having respiratory control and a tolerance to calcium. Biochem Biophys Res Commun 72: 327-333, 1976.
71. Raza A, Franklin MJ, Dudek AZ. Pericytes and vessel maturation during tumor angiogenesis and metastasis. Am J Hematol 85: 593-598, 2010.
72. Reynolds LP, Grazul-Bilska AT, Redmer DA. Angiogenesis in the corpus luteum. Endocrine 12: 1-9, 2000.
73. Ribatti D, Nico B, Crivellato E. The role of pericytes in angiogenesis. Int J Dev Biol 55: 261-268, 2011.
74. Romanul FC, Bannister RG. Localized areas of high alkaline phosphatase activity in the terminal arterial tree. J Cell Biol 15: 73-84, 1962.
75. Santiago A, Satriano J, DeCandido S, Holthofer H, Schreiber R, Unkeless J, Schlondorff D. A specific Fc gamma receptor on cultured rat mesangial cells. J Immunol 143: 2575-2582, 1989.
76. Scholz T, Temmler U, Krause S, Heptinstall S, Losche W. Transfer of tissue factor from platelets to monocytes: role of platelet-derived mi-crovesicles and CD62P. Thromb Haemost 88: 1033-1038, 2002.
77. Segal SS. Frontiers in microcirculation: control processes and clinical applications. Microcirculation 17: 159-163, 2010.
78. Segal SS. Integration of blood flow control to skeletal muscle: key role of feed arteries. Acta Physiol Scand 168: 511-518, 2000.
79. Segal SS. Regulation of blood flow in the microcirculation. Microcirculation 12: 33-45, 2005.
80. Segal SS, Damon DN, Duling BR. Propagation of vasomotor responses coordinates arteriolar resistances. Am J Physiol Heart Circ Physiol 256: H832-H837, 1989.
81. Segal SS, Duling BR. Conduction of vasomotor responses in arterioles: a role for cell-to-cell coupling? Am J Physiol Heart Circ Physiol 256: H838-H845, 1989.
82. Segal SS, Welsh DG, Kurjiaka DT. Spread of vasodilatation and vasoconstriction along feed arteries and arterioles of hamster skeletal muscle. J Physiol 516: 283-291, 1999.
83. Shepro D, Morel NM. Pericyte physiology. FASEB J 7: 1031-1038, 1993.
84. Sims DE. Recent advances in pericyte biology-implications for health and disease. Can J Cardiol 7: 431-443, 1991.
85. + perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol 7: 870-879, 2005.
86. Szabo A, Mehes E, Kosa E, Czirok A. Multicellular sprouting in vitro. Biophys J 95: 2702-2710, 2008.
87. Thanabalasundaram G, Schneidewind J, Pieper C, Galla HJ. The impact of pericytes on the blood-brain barrier integrity depends critically on the pericyte differentiation stage. Int J Biochem Cell Biol 43: 1284-1293, 2011.
88. Tracy PB, Robinson RA, Worfolk LA, Allen DH. Procoagulant activities expressed by peripheral blood mononuclear cells. Methods Enzymol 222: 281-299, 1993.
89. + channels involvement in capillary sensing and for bidirectionality in capillary communication. Microvasc Res 53: 245-253, 1997.
90. Ucuzian AA, Greisler HP. In vitro models of angiogenesis. World J Surg 31: 654-663, 2007.
91. Valarmathi MT, Davis JM, Yost MJ, Goodwin RL, Potts JD. A three-dimensional model of vasculogenesis. Biomaterials 30: 1098-1112, 2009.
92. Viles-Gonzalez JF, Fuster V, Badimon JJ. Links between inflammation and thrombogenicity in atherosclerosis. Curr Mol Med 6: 489-499, 2006.
93. + current in single, cultured pericytes from bovine heart. Cardiovasc Res 46: 569-578, 2000.
94. von Tell D, Armulik A, Betsholtz C. Pericytes and vascular stability. Exp Cell Res 312: 623-629, 2006.
95. Weibel ER. On pericytes, particularly their existence on lung capillaries. Microvasc Res 8: 218-235, 1974.
96. Weiskirchen R, Gressner AM. Isolation and culture of hepatic stellate cells. Methods Mol Med 117: 99-113, 2005.
97. Weiss DR, Juchem G, Kemkes BM, Gansera B, Nees S. Extensive deendothelialization and thrombogenicity in routinely prepared vein grafts for coronary bypass operations: facts and remedy. Int J Clin Exp Med 2: 95-113, 2009.
98. Winkler EA, Bell RD, Zlokovic BV. Pericyte-specific expression of PDGF beta receptor in mouse models with normal and deficient PDGF beta receptor signaling. Mol Neurodegener 5: 32, 2010.
99. Wood W, Martin P. Structures in focus-filopodia. Int J Biochem Cell Biol 34: 726-730, 2002.
100. Yamagishi S, Imaizumi T. Pericyte biology and diseases. Int J Tissue React 27: 125-135, 2005.
101. Yeh HI, Rothery S, Dupont E, Coppen SR, Severs NJ. Individual gap junction plaques contain multiple connexins in arterial endothelium. Circ Res 83: 1248-1263, 1998.
102. Zimmermann KW. Der feinere Bau der Blutcapillaren. Zeitschr f d ges Anat 68: 29-109, 1923.