References
Addison DJ, Garner A, Ashton N (1970) Degeneration of intramural pericytes in diabetic retinopathy. Br Med J 1:264–266
Akagi Y, Kador PF (1990) Effect of aldose reductase inhibitors on the progression of retinopathy in galactose-fed dogs. Exp Eye Res 50:635–639
Antonelli-Orlidge A, Saunders KB, Smith SR, D'Amore PA (1989) An activated form of transforming growth factor β is produced by cocultures of endothelial cells and pericytes. Proc Natl Acad Sci USA 86:4544–4548
Archer DB, Gardiner TA (1981) Electron microscopic features of experimental choroidal neovascularization. Am J Ophthalmol 91:433–457
Ashton N, DeOliveira F (1966) Nomenclature of pericytes. Intramural and extramural. Br J Ophthalmol 50:119–123
Ausprunk DH, Folkman J (1977) Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res 14:53–65
Balin BJ, Broadwell RD, Salcman M, El-Kalliny M (1986) Avenues for entry of peripherally administered protein to the central nervous system in mouse, rat, and squirrel monkey. J Comp Neurol 251:260–280
Bär T, Wolff JR (1972) The formation of capillary basement membranes during internal vascularization of the rat's cerebral cortex. Z Zellforsch 133:231–248
Blood CH, Zetter BR (1990) Tumor interactions with the vasculature: angiogenesis and tumor metastasis. Biochim Biophys Acta 1032:89–118
Bloodworth JMB Jr, Molitor DL (1965) Ultrastructural aspects of human and canine diabetic retinopathy. Invest Ophthalmol Vis Sci 4:1037–1048
Braverman IM, Sibley J, Keh A (1990) Ultrastructural analysis of the endothelial-pericyte relationship in diabetic cutaneous vessels. J Invest Dermatol 95:147–153
Broadwell RD, Salcman M (1981) Expanding the definition of the blood-brain barrier to protein. Proc Natl Acad Sci USA 78:7820–7824
Buzney SM, Frank RN (1975) Retinal capillaries: proliferation of mural cells in vitro. Science 190:985–986
Buzney SM, Frank RN, Varma SD, Tanishima T, Gabbay KH (1977) Aldose reductase in retinal mural cells. Invest Ophthalmol Vis Sci 16:392–396
Buzney SM, Massicotte SJ, Hetu N, Zetter BR (1983) Retinal vascular endothelial cells and pericytes — Differential growth characteristics in vitro. Invest Ophthalmol Vis Sci 24:470–480
Cancilla PA, Baker RN, Pollock PS, Frommes BS (1972) The reaction of pericytes of the central nervous system to exogenous protein. Lab Invest 26:376–383
Canfield AE, Allen TD, Grant ME, Schor SL, Schor AM (1990) Modulation of extracellular matrix biosynthesis by bovine retinal pericytes in vitro: effects of the substratum and cell density. J Cell Sci 96:159–169
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
Carlson EC, Bjork NJ (1990) SEM and TEM analyses of isolated human retinal microvessel basement membranes in diabetic retinopathy. Anat Rec 226:295–306
Carlson EC, Audette JL, Swinscoe JC (1988) Ultrastructural evidence for morphological specificity in isolated bovine retinal capillary basement membranes. J Ultrastruct Mol Struct Res 98:184–198
Carson MP, Haudenschild CC (1986) Microvascular endothelium and pericytes: high yield, low passage cultures. In Vitro Cell Dev Biol 22:344–354
Cavallo T, Sade R, Folkman J, Cotran RS (1972) Tumor angiogenesis. Rapid induction of endothelial mitoses demonstrated by autoradiography. J Cell Biol 54:408–420
Cavallo T, Sade R, Folkman J, Cotran RS (1973) Ultrastructural autoradiographic studies of the early vasoproliferative response in tumor angiogenesis. Am J Pathol 70:345–362
Clark ER, Clark EL (1925) A. The development of adventitial (rouget) cells on the blood capillaries of amphibian larvae. Am J Anat 35:239–264
Cliff WJ (1963) Observations on healing tissue: A combined light and electron microscopic investigation. Philos Trans R Soc London 246:305–325
Cohen MP, Frank RN, Khalifa AA (1980) Collagen production by cultured retinal capillary pericytes. Invest Ophthalmol Vis Sci 19:90–94
Crocker DJ, Murad TM, Geer JC (1970) Role of the pericyte in wound healing. An ultrastructural study. Exp Mol Pathol 13:51–65
Darby I, Skalli O, Gabbiani G (1990) α-Smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Invest 63:21–29
Dennis PA, Rifkin DB (1991) Cellular activation of latent transforming growth factor β requires binding to the cation-independent mannose 6-phosphate/insulin-like growth factor type II receptor. Proc Natl Acad Sci USA 88:580–584
DeOliveira F (1966) Pericytes in diabetic retinopathy. Br J Ophthalmol 50:134–143
Dermietzel R, Krause D (1991) Molecular anatomy of the blood-brain barrier as defined by immunocytochemistry. Int Rev Cytol 127:57–109
Díaz-Flores L, Gutiérrez R, Varela H, Rancel N, Valladares F (1991) Microvascular pericytes: a review of their morphological and functional characteristics. Histol Histopathol 6:269–286
Dodge AB, Hechtman HB, Shepro D (1991) Microvascular endothelial-derived autacoids regulate pericyte contractility. Cell Motil Cytoskelet 18:180–188
Drenckhahn D (1982) Localization of contractile proteins in endothelial cells and pericytes. Drug Res 32:1344–1345
Drenckhahn D, Schnittler H, Nobiling R, Kriz W (1990) Ultrastructural organization of contractile proteins in rat glomerular mesangial cells. Am J Pathol 137:1343–1351
Elger M, Drenckhahn D, Nobiling R, Mundel P, Kriz W (1993) Cultured rat mesangial cells contain smooth muscle α-actin not found in vivo, Am J Pathol (in press)
Engerman RL, Bloodworth JMB Jr (1965) Experimental diabetic retinopathy in dogs. Arch Ophthalmol 73:205–210
Engerman RL, Kern TS (1984) Experimental galactosemia produces diabetic-like retinopathy. Diabetes 33:97–100
Farrell CR, Stewart PA, Farrell CL, DelMaestro RF (1987) Pericytes in human cerebral microvasculature. Anat Rec 218:466–469
Folkman J (1984) What is the role of endothelial cells in angiogenesis? Lab Invest 51:601–604
Folkman J, Shing Y (1992) Angiogenesis (review). J Biol Chem 267:10931–10934
Forbes MS, Rennels ML, Nelson E (1976) Ultrastructure of pericytes in mouse heart. Am J Anat 149:47–70
Frank RN, Keirn RJ, Kennedy A, Frank KW (1983) Galactose-induced retinal capillary basement membrane thickening: prevention by sorbinil. Invest Ophthalmol Vis Sci 24:1519–1524
Frank RN, Dutta S, Mancini MA (1987) Pericyte coverage is greater in the retinal than in the cerebral capillaries of the rat. Invest Ophthalmol Vis Sci 28:1086–1091
Frank RN, Turczyn TJ, Das A (1990) Pericyte coverage of retinal and cerebral capillaries. Invest Ophthalmol Vis Sci 31:999–1007
Frey A, Meckelein B, Weiler-Güttler H, Möckel B, Flach R, Gassen HG (1991) Pericytes of the brain microvasculature express γ-glutamyltranspeptidase. Eur J Biochem 202:421–429
Fujimoto T, Singer SJ (1987) Immunocytochemical studies of desmin and vimentin in pericapillary cells of chicken. J Histochem Cytochem 35:1105–1115
Furcht LT (1986) Critical factors controlling angiogenesis: cell products, cell matrix, and growth factors (editorial). Lab Invest 55:505–509
Gitlin JD, D'Amore PA (1983) Culture of retinal capillary cells using selective growth media. Microvasc Res 26:74–80
Herman IM, D'Amore PA (1985) Microvascular pericytes contain muscle and nonmuscle actins. J Cell Biol 101:43–52
Imayama S, Urabe H (1984) Pericytes on the dermal microvasculature of the rat skin. Anat Embryol 169:271–274
Ishibashi T, Miller H, Orr G, Sorgente N, Ryan SJ (1987) Morphologic observations on experimental subretinal neovascularization in the monkey. Invest Ophthalmol Vis Sci 28:1116–1130
Johnson RJ, Iida H, Alpers CE, Majesky MW, Schwartz SM, Pritzl P, Gordon K, Gown AM (1991) Expression of smooth muscle cell phenotype by rat mesangial cells in immune complex nephritis. J Clin Invest 87:847–858
Jotereau FV, LeDouarin NM (1978) The developmental relationship between osteocytes and osteoclasts: A study using the quail-chick nuclear marker in endochondral ossification. Dev Biol 63:253–265
Joyce NC, DeCamilli P, Boyles J (1984) Pericytes, like vascular smooth muscle cells, are immunocytochemically positive for cyclic GMP-dependent protein kinase. Microvasc Res 28:206–219
Joyce NC, DeCamilli P, Lohmann SM, Walter U (1986) cGMP-dependent protein kinase is present in high concentrations in contractile cells of the kidney vasculature. J Cyclic Nucleotide Protein Phosphor Res 11:191–198
Joyce NC, Haire MF, Palade GE (1985a) Contractile proteins in pericytes. I. Immunoperoxidase localization of tropomyosin. J Cell Biol 100:1379–1386
Joyce NC, Haire MF, Palade GE (1985b) Contractile proteins in pericytes. II. Immunocytochemical evidence for the presence of two isomyosins in graded concentrations. J Cell Biol 100:1387–1395
Kapanci J, Burgan S, Pietra GG, Conne B, Gabbiani G (1990) Modulation of actin isoform expression in alveolar myofibroblasts (contractile interstitial cells) during pulmonary hypertension. Am J Pathol 136:881–889
Kawasaki S, Mori M, Awai M (1989) Capillary growth of rat aortic segments cultured in collagen gel without serum. Acta Pathol Jpn 39:712–718
Kelley C, D'Amore P, Hechtman HB, Shepro D (1987) Microvascular pericyte contractility in vitro: comparison with other cells of the vascular wall. J Cell Biol 104:483–490
Kennedy A, Frank RN, Varma SD (1983) Aldose reductase activity in retinal and cerebral microvessels and cultured vascular cells. Invest Ophthalmol Vis Sci 24:1250–1258
Kenney AJ, Turner AJ (eds) (1987) Mammalian ectoenzymes. Elsevier, Amsterdam
Klagsbrun M, D'Amore PA (1991) Regulators of angiogenesis. Annu Rev Physiol 53:217–239
Komuro T (1990) Re-evaluation of fibroblasts and fibroblast-like cells. Anat Embryol 182:103–112
Krause D, Vatter B, Dermietzel R (1988) Immunochemical and immunocytochemical characterization of a novel monoclonal antibody recognizing a 140 kDa protein in cerebral pericytes of the rat. Cell Tissue Res 252:543–555
Krause D, Kunz J, Dermietzel R (1992) Cerebral pericytes — a second line of defence in controlling blood-brain barrier peptide metabolism. In: Drewes LR, Betz AL (eds) Frontiers in cerebral vascular biology: transport and its regulation. Plenum Press, New York (in press)
Kuwabara T, Cogan DG (1963) Retinal vascular patterns. VI. Mural cells of the retinal capillaries. Arch Ophthalmol 69:492–502
Laties AM, Rapoport SI, McGlinn A (1979) Hypertensive breakdown of cerebral but not of retinal blood vessels in rhesus monkey. Arch Ophthalmol 97:1511–1514
Majno G (1965) Ultrastructure of the vascular membrane. In: Hamilton WF, Dowie P (eds) Handbook of physiology, section 2: Circulation American Physiological Society, Washington, pp 2293–2375
Matsusaka T (1970) Ultrastructural differences between the choriocapillaris and retinal capillaries on the human eye. Jpn J Ophthalmol 14:58–71
Mazanet R, Franzini-Armstrong C (1982) Scanning electron microscopy of pericytes in rat red muscle. Microvasc Res 23:361–369
McCuskey RS, Chapman TM (1969) Microscopy of the living pancreas in situ. Am J Anat 126:395–408
Meyrick B, Reid L (1978) The effect of continued hypoxia on rat pulmonary arterial circulation. Lab Invest 38:188–200
Nakayasu K (1988) Origin of pericytes in neovascularization of rat cornea. Jpn J Ophthalmol 32:105–112
Nehls V, Drenckhahn D (1991a) Demonstration of actin filament stress fibers in microvascular endothelial cells in situ. Microvasc Res 42:103–112
Nehls V, Drenckhahn D (1991b) Heterogeneity of microvascular pericytes for smooth muscle type alpha-actin. J Cell Biol 113:147–154
Nehls V, Denzer K, Drenckhahn D (1992) Pericyte involvement in capillary sprouting during angiogenesis in situ. Cell Tissue Res 270:469–474
Orlidge A, D'Amore PA (1987) Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J Cell Biol 105:1455–1462
Paku S, Paweletz N (1991) First steps of tumor-related angiogenesis. Lab Invest 65:334–346
Patz A, Maumenee AE (1962) Studies on diabetic retinopathy. Am J Ophthalmol 54:532–541
Paweletz N, Knierim M (1989) Tumor-related angiogenesis. Crit Rev Oncol Hematol 9:197–242
Rhodin JAG, Fujita H (1989) Capillary growth in the mesentery of normal young rats. Intravital video and electron microscope analysis. J Submicrosc Cytol Pathol 21:1–34
Risau W, Dingler A, Albrecht U, Dehouck MP, Cecchelli R (1992) Blood-brain barrier pericytes are the main source of γ-glutamyltranspeptidase activity in brain capillaries. J Neurochem 98:667–672
Robison WG Jr, Nagata M, Tillis TN, Laver N, Kinoshita JH (1989a) Aldose reductase and pericyte-endothelial cell contacts in retina and optic nerve. Invest Ophthalmol Vis Sci 30:2293–2299
Robison WG Jr, Nagata M, Laver N, Hohman TC, Kinoshita JH (1989b) Diabetic-like retinopathy in rats prevented with an aldose reductase inhibitor. Invest Ophthalmol Vis Sci 30:2285–2292
Robison WG Jr, McCaleb ML, Feld LG, Michaelis OE, Laver N, Mercandetti M (1991) Degenerated intramural pericytes (‘ghost cells’) in the retinal capillaries of diabetic rats. Curr Eye Res 10:339–350
Rønnov-Jessen L, Celis JE, VanDeurs B, Petersen OW (1992) A fibroblast-associated antigen: characterization in fibroblasts and immunoreactivity in smooth muscle differentiated stromal cells. J Histochem Cytochem 40:475–486
Rouget C (1873) Mémoire sur le dévelopement, la structure et les propriétés physiologiques des capillaires sanguins et lymphatiques. Arch Physiol Norm Pathol 5:603–663
Sappino AP, Schürch W, Gabbiani G (1990a) Biology of disease: differentiation repertoire of fibroblastic cells: expression of cytoskeletal proteins as marker of phenotypic modulations. Lab Invest 63:144–161
Sappino AP, Masouye I, Saurat JH, Gabbiani G (1990b) Smooth muscle differentiation in scleroderma fibroblastic cells. Am J Pathol 137:585–591
Sato N, Sawasaki Y, Senoo A, Fuse Y, Hirano Y, Goto T (1987) Development of capillary networks from rat microvascular fragments in vitro: the role of myofibroblastic cells. Microvasc Res 33:194–210
Sato Y, Rifkin DB (1989) Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-β1-like molecule by plasmin during co-culture. J Cell Biol 109:309–315
Sato Y, Tsuboi R, Lyons R, Moses H, Rifkin DB (1990) Characterization of the activation of latent TGF-β by cocultures of endothelial cells and pericytes or smooth muscle cells: a self-regulating system. J Cell Biol 111:757–763
Schlingemann RO, Rietveld FJR, Kwaspen F, Van DeKerkhof PCM, DeWaal RMW, Ruiter DJ (1991) Differential expression of markers for endothelial cells, pericytes, and basal lamina in the microvasculature of tumors and granulation tissue. Am J Pathol 138:1335–1347
Schlöndorff D (1987) The glomerular mesangial cell: an expanding role for a specialized pericyte. FASEB J 1:272–281
Schor AM, Schor SL (1986) The isolation and culture of endothelial cells and pericytes from the bovine retinal microvasculature: a comparative study with large vessel vascular cells. Microvasc Res 32:21–38
Schor AM, Schor SL (1983) Tumor angiogenesis. J Pathol 141:385–413
Schürch W, Skalli O, Seemayer TA, Gabbiani G (1987) Intermediate filament proteins and actin isoforms as markers for soft tissue tumor differentiation and origin. Am J Pathol 128:91–103
Sima AAF, Chakrabarti S, Garcia-Salinas R, Basu PK (1985) The BB-rat — an authentic model of human diabetic retinopathy. Curr Eye Res 4:1087–1092
Sims DE (1986) The pericyte — a review. Tissue Cell 18:153–174
Sims DE, Miller FN, Donald A, Perricone MA (1990) Ultrastructure of pericytes in early stages of histamine-induced inflammation. J Morphol 206:333–342
Singer KH, Searce RM, Tuck DT, Whichard LP, Denning SM, Haynes BF (1989) Removal of fibroblasts from human epithelial cell cultures with use of a complement fixing monoclonal antibody reactive with human fibroblasts and monocytes/macrophages. J Invest Dermatol 92:166–170
Skalli O, Pelte MF, Peclet MC, Gabbiani G, Gugliotta P, Bussolati G, Ravazzola M, Orci L (1989a) α-Smooth muscle actin, a differentiation marker of smooth muscle cells, is present in microfilamentous bundles of pericytes. J Histochem Cytochem 37:315–321
Skalli O, Gabbiani G (1986) The biology of the myofibroblast in relation to wound contraction and fibrocontractive diseases. In: Clark R, Henson P (eds) The molecular and cellular biology of wound repair. Plenum, New York, pp 3–36
Skalli O, Ropraz P, Trzeciak A, Benzonana G, Gillessen D, Gabbiani G (1986) A monclonal antibody against α-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol 103:2787–2796
Skalli O, Schürch W, Seemayer T, Lagacé R, Montandon D, Pittet B, Gabbiani G (1989b) Myofibroblasts from diverse pathologic settings are heterogeneous in their content of actin isoforms and intermediate filament proteins. Lab Invest 60:275–285
Skalli O, Vandekerckhove J, Gabbiani G (1987) Actin-isoform pattern as a marker of normal or pathological smooth-muscle and fibroblastic tissues. Differentiation 33:232–238
Speiser P, Gittelsohn AM, Patz A (1968) Studies on diabetic retinopathy. Arch Ophthalmol 80:332–337
Swinscoe JC, Meyer DA, Carlson EC (1990) Bovine retinal microvessel endothelial cells secrete factors which stimulate pericyte proliferation and contraction. J Cell Biol 111:183a
Tilton RG, Kilo C, Williamson JR, Murch DW (1979) Differences in pericyte contractile function in rat cardiac and skeletal muscle microvasculatures. Microvasc Res 18:336–352
Tilton RG, Hoffmann PL, Kilo C, Williamson JR (1981) Pericyte degeneration and basement membrane thickening in skeletal muscle capillaries of human diabetics. Diabetes 30:326–334
Tilton RG, LaRose LS, Kilo C, Williamson JR (1986) Absence of degenerative changes in retinal and uveal capillary pericytes in diabetic rats. Invest Ophthalmol Vis Sci 27:716–721
Toussaint D, Dustin P (1963) Electron microscopy of normal and diabetic retinal capillaries. Arch Ophthalmol 70:96–108
Van Deurs B (1976) Observations on the blood-brain barrier in hypertensive rats, with particular reference to phagocytic pericytes. J Ultrastruct Res 56:65–77
Verhoeven D, Buyssens N (1988) Desmin-positive stellate cells associated with angiogenesis in a tumour and non-tumour system. Virchows Arch [Cell Pathol] 54:263–272
Vimtrup B (1922) Beiträge zur Anatomie der Capillaren. I. Über contractile Elemente in der Gefäßwand der Blutcapillaren. Z Anat Entw Gesch 65:150–184
Vracko R, Benditt EP (1970) Capillary basal lamina thickening. J Cell Biol 47:281–285
Wakui S (1988) Two- and three-dimensional ultrastructural observation of two cell angiogenesis in human granulation tissue. Virchows Arch [Cell Pathol] 56:127–139
Weibel ER (1974) On pericytes, particularly their existence on lung capillaries. Microvasc Res 8:218–235
Weigelt H, Addicks K, Hauck G, Lübbers DW (1979) Vital microscopic studies in regard to the role of intraendothelial reactive structures in the inflammatory process. Bibl Anat 17:11–20
Yamashita T, Becker B (1961) Basement membrane in human diabetic eye. Diabetes 10:167–174
Yanoff M (1966) Diabetic retinopathy. N Engl J Med 274:1344–1349
Zimmermann KW (1923) Der feinere Bau der Blutcapillaren. Z Anat Entw Gesch 68:3–109
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Nehls, V., Drenckhahn, D. The versatility of microvascular pericytes: from mesenchyme to smooth muscle?. Histochemistry 99, 1–12 (1993). https://doi.org/10.1007/BF00268014
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DOI: https://doi.org/10.1007/BF00268014