Ultrastructural pathology of cortical capillary pericytes in human traumatic brain oedema

Folia Neuropathologica

Volumn 49, Issue 3, 2011, Pages 162-173

  Castejón, Orlando J ^a  

^a UNIVERSIDAD DEL ZULIA   (Venezuela)

Author keywords

Brain oedema; Brain trauma; Cerebral cortex; Electron microscopy; Pericytes

Indexed keywords

ACTIN; GLYCOGEN; MYOSIN;

ACTIN FILAMENT; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN EDEMA; CELL INTERACTION; CELL VACUOLE; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; GOLGI COMPLEX; HUMAN; HYPERTROPHY; PERICYTE; PHAGOCYTOSIS; PINOCYTOSIS; REVIEW; TRAUMATIC BRAIN INJURY; ULTRASTRUCTURE;

EID: 80053529558     PISSN: 16414640     EISSN: 1509572X     Source Type: Journal    
DOI: None     Document Type: Review

References (75)

1. Addison DJ, Garner A, Ashton N. Degeneration of intramural pericytes in diabetic retinopathy. Br Med J 1970; 31: 264-266.
2. Allt G, Lawrenson JG. Pericytes: cell biology and pathology. Cell Tissues Organs 2001; 169: 1-11. (Pubitemid 32437039)
3. Ammoury A, Michaud S, Paul C, Prost-Squarcioni C, Alvarez F, Lamant L, Launay F, Bazex J, Chouini-Lalanne N, Marguery MC. Photodistribution of blue-gray hyperpigmentation after amiodarone treatment: molecular characterization of amiodarone in the skin. Arch Dermatol 2008; 144: 92-96. (Pubitemid 351159394)
4. Baron M, Gallego A. The relationship of the microglia with the pericytes in the cat cerebral cortex. Z Zellforsch 1972; 128: 42-57.
5. Bertossi M, Virgintino D, Majorano E, Occhiogrosso M, Roncali L. Ultrastructural and morphometric investigation of human brain capillaries in normal and peritumoral tissues. Ultrastruct Pathol 1997; 21: 41-49. (Pubitemid 27099728)
6. Brierley JB, Brown AW. The origin of lipid phagocytes in the central nervous system: II. The adventitia of blood vessels. J Comp Neurol 1982; 211: 407-417. (Pubitemid 13250706)
7. Cammermeyer J. Juxtavascular karyokinesis and microglia cell proliferation during retrograde reaction in the mouse facial nucleus. Ergeb Anat Entwuiklungsgesch 1965; 38: 1-22.
8. Cancilla PA, Baker RN, Pollock PS, Frommes SP. The reaction of pericytes of the central nervous system to exogenous protein. Lab Invest 1972; 26: 376-383.
9. Castejón OJ. Electron microscopic study of capillary wall in human cerebral edema. J Neuropathol Exp Neurol 1980; 39: 296-328. (Pubitemid 10100467)
10. Castejón OJ. Submicroscopic changes of cortical capillary pericytes in human perifocal brain edema. J Submicrosc Cytol 1984; 16: 601-618.
11. De Gracia DJ, Kreipke CW, Kayali FM, Rafols JA. Brain endothelial HSP-70 stress response coincides with endothelial and pericyte death after brain trauma. Neurol Res 2007; 29: 356-361. (Pubitemid 47196053)
12. Desaki J, Nishida N. A further observation of the structural changes of microvessels in the extensor digitorum longus muscle of the aged rat. J Electron Microsc (Tokyo) 2007; 56: 249-255.
13. Dodson RE, Aoyagi M, Chu LW-F. Ultrastructural changes in subacute cerebral infarction following middle cerebral artery occlusion in the baboon. Cytobios 1975; 13: 97-108.
14. Dodson RE, Tagashira Y, Chu LW-F. Acute pericyte response to cerebral ischemia. J Neurol Sci 1976; 29: 9-16.
15. Dore-Duffy P, Owen C, Balabanov R, Murphy S, Beaumont T, Rafols JA. Pericyte migration from the vascular wall in response to traumatic brain injury. Microvasc Res 2000; 60: 55-69. (Pubitemid 30456828)
16. Dore-Duffy P, Wang X, Mehedi A, Kreripke CW, Rafols JA. Differential expression of capillary VEGF isoforms following traumatic brain injury. Neurol Res 2007; 29: 395-403. (Pubitemid 47196059)
17. Farquhar MG, Hartmann JF. Electron microscopy of cerebral capillaries. J Neuropathol Exp Neurol 1956; 15: 18-39.
18. Fisher M, French S, Ji P, Kim RC. Cerebral microbleeds in the elderly: a pathological analysis. Stroke 2010; 41: 2782-2875.
19. Frey A, Meckelein B, Weiler-Guttler H, Mockel B, Flach R, Gassen HG. Pericytes of the brain microvasculature express gammaglutamyl transpeptidase. Eur J Biochem 1991; 202: 421-429.
20. Frontczak-Baniewicz J, Olszewska H, Gadamski R, Barskow I, Gajkowska B. Alterations in rat's brain capillaries in a model of focal cerebral necrosis. Exp Toxicol Pathol 2000; 52: 77-85. (Pubitemid 30176954)
21. Glees P, Hasan M, Voth D, Schwarz M. Fine structural features of the cerebral microvaculature in hydrocephalic human infants: correlated clinical observations. Neurosurg Rev 1989; 12: 315-321. (Pubitemid 19278087)
22. Hayden MR, Karuparthi PR, Habibi J, Wasekar C, Lastra G, Manrique C, Stas S, Sowers JR. Ultrastructural islet study of early fibrosis in the Ren2 rat model of hypertension. Emerging role of the islet pancreatic pericyte-stellate cell. JOP 2009; 8: 725-738. (Pubitemid 350200191)
23. Hayden MR, Karuparthi PR, Habibi J, Lastra G, Patel K, Wase - kar C, Manrique CM, Ozerdem U, Stas S, Sowers JR. Ultrastructure of islet microcirculation, pericytes and the islet exocrine interface in the HIP rat model of diabetes. Exp Biol Med 2008; 233: 1109-1123.
24. Hayden MR, Patel K, Habibi J, Gupta D, Tekwani SS, Whaley- Connell A, Sowers JR. Attenuation of endocrine-exocrine pancreatic communication in type 2 diabetes: pancreatic extracellular matrix ultrastructural abnormalities. J Cardiometab Syndr 2008; 3: 234-243.
25. Gerrits PO, De Weerd H, van der Want JJ, Kortekaas R, Luiten PG, Veening JG. Microvascular changes in estrogen-á sensitive brainstem structures of aging female hamsters. Neurosci Res 2010; 67: 267-274.
26. Gonul E, Duz B, Kahraman S, Kayali H, Kubar A, Tumurkaynak E. Early pericyte response to brain hypoxia in cats: an ultrastructural study. Microvasc Res 2002; 64: 116-119. (Pubitemid 34713237)
27. Hayashi K, Nakao S, Nakaoke R, Nakagawa S, Kitagawa N, Niwa M. Effects of hypoxia on endotelial/pericytic co-culture modelo f the blood-brain barrier. Regul Pept 2004; 123: 77-83. (Pubitemid 39424152)
28. Herman IJ, Jacobson S. In situ analysis of microvasculr pericytes in hypertensive rat brain. Tissue Cell 1988; 20: 1-12. (Pubitemid 18084546)
29. Herman IM, Newcomb PM, Coughlin JE, Jacobson S. Characterization of microsvascular cell cultures from normotensive and hypertensive rat brains: pericyte-endothelial cell interactions in vitro. Tissue Cell 1987; 19: 197-206. (Pubitemid 17060161)
30. Hills CP. Ultrastructural changes in the capillary bed of the rat cerebral cortex in anoxic-ischemic brain lesions. Am J Pathol 1964; 44: 531-544.
31. Jeynes B. Reactions of granular pericytes in a rabbit cerebrovascular ischemia model. Stroke 1985; 16: 121-125. (Pubitemid 15194769)
32. Kitamura T. The origin of brain macrophages. Some cosiderations on the microglia theory of Del Rio Hortega. Acta Pathol Jpn 1973; 23: 11-26.
33. Kosunen TU, Waksman BH, Samuelsson IK. Radioautographic study of cellular mechanisms in delayed hypersensitivity. J Neuropathol Exp Neurol 1963; 22: 367-380.
34. Lafarga M, Palacios G. Ultrastructural study of pericytes in the rat supraoptic nucleus. J Anat 1975; 120: 433-438.
35. Le Beux YJ, Willemot J. Actin-like filaments in the endothelial cells of adult rat brain capillaries. Exp Neurol 1978a; 58: 446-454. (Pubitemid 8277328)
36. Le Beux YJ, Willemot J. Actin and myosin-like filaments in rat brain pericytes. Anat Rec 1978b; 190: 811-826. (Pubitemid 8340598)
37. Lewandowska E, Szpak GM, Wierzba-Bobrowicz T, Modzelewska J, Stȩpień T, Pasennik E, Schmidt-Sidor B, Rafałowska J. Capillary vessel wall in CADASIL angiopathy. Folia Neuropathol 2010; 48: 104-115.
38. Li C, Zhang WF, Zhao YF. Pericytes may have important role in the pathogenesis of vascular malformation. Med Hypothesis 2007; 68: 808-810.
39. Li YJ, Wen G, Yang L, Zhang XL. Heterogeneity of angioarchitecture and their hemodynamic changes in benign and malignant breast tumors. Zhonghua Zhong Liu Za Zhi 2009; 31: 24-27.
40. Liwnicz BH, Leach JL, Yeh HS, Privitera M. Pericyte degeneration and thickening of basement membranes of cerebral microvessels in complex partial seizures: electron microscopic study of surgically removed tissue. Neurosurgery 1990; 26: 409-420. (Pubitemid 20092853)
41. Liu HM. Neovascullature and blood-brain barrier in ischemic brain infarct. Acta Neuropathol 1988; 75: 422-426.
42. Lupo G, Anfuso CD, Assero G, Strosznajder RP, Walski M, Pluta R, Alberghina M. Amyloid beta (1-42) and its beta (25-35) fragment induce in vitro phosphatidylcholine hydrolysis in bovine retina capillary pericytes. Neurosci Lett 2001; 303: 185-188. (Pubitemid 32373286)
43. Majno G, Shea SM, Leventhal M. Endothelial contraction induced by histamine type mediators. J Cell Biol 1969; 42: 647-672.
44. Markov DV, Dimova RN. Ultrastructural alteration of rat brain microglia cells and pericytes after chronic lead poisoning. Acta Neuropathol (Berlin) 1974; 28: 25-35.
45. Mato M, Ookawara S, Kurihora K. Uptake of exogenous substances and marked infoldings of the fluorescent granular pericytes in cerebral fine vessels. Am J Anat 1980; 157: 329-332. (Pubitemid 10076854)
46. Maxwell DS, Kruger L. Small blood vessels and the origin of phagocytes in the rat cerebral cortex following heavy particle irradiation. Exp Neurol 1965; 12: 33-54.
47. Maynard EA, Schultz RL, Peace DC. Electron microscopy of the vascular bed of the rat cerebral cortex. Am J Anat 1957; 100: 409-433.
48. Mc Donald LW, Hayes L. The role of capillaries in the pathogenesis of delayed radionecrosis of brain. Am J Pathol 1967; 50: 745-764.
49. Medrado A, Costa T, Prado T, Reis S, Andrade Z. Phenotype characterization of pericytes during tissue repair following low-level laser therapy. Photodermatol Photoimmunol Photomed 2010; 2: 192-197.
50. Melgar MA, Rafols J, Gloss D, Diaz FG. Postischemic reperfusion: ultrastructural blood-brain barrier and hemodynamic correlative changes in an awake model of transient forebrain ischemia. Neurosurgery 2005; 56: 571-581.
51. Mori S, Leblond CP. Identification of microglia in light and electron microscopy. J Comp Neurol 1969; 135: 57-80.
52. Owman Ch, Edvinsson L, Hardebo JE, Croshel-Stewari U, Unsicker K, Walles B. Immunohistochemical demonstration of actin and myosin in brain capillaries. In: Cervós-Navarro J, Betz E, Ebhardt G, Ferst R, Wullemweber R (eds.). Advances in Neurology. Vol. 20. Raven Press, New York 1978; pp. 347-352.
53. Pavlov KA, Chekmaryova IA, Shchyogolev AI, Mishnyov OD. Ultrastructural characteristics of peripheral arteriovenous and venous angiodysplasias. Bull Exp Biol Med 2009; 147: 480-484.
54. Perimutter LS. Microvascular pathology and vascular basement membrane components in Alzheimer's disease. Mol Neurobiol 1994; 9: 33-40.
55. Persson L. Cellular reactions to small cerebral stab wounds in the rat frontal lobe. An ultrastructural study. Virchows Arch B Cell Pathol 1976; 18: 21-37.
56. Piquer-Gil M, García-Verdugo JM, Zipancic I, Sánchez MJ, Alvarez-Dolado M. Cell fusion contributes to pericyte formation after stroke. J Cereb Blood Flow Metab 2009; 29: 480-485.
57. Popova EN, Zagrebina OV. Ultrastructure of the blood-brain barrier in the cerebral cortex in atherosclerotic dementia. Morfologiia 1998; 114: 25-30.
58. Rensink AA, Otte-Holler I, De Boer R, Bosch RR, Ten Donkelaar HJ, De Waal RM, Verbeek MM, Kremer B. Insulin inhibits amyloid beta-induced cell death in cultured human brain pericytes. Neurobiol Aging 2004; 25: 93-103. (Pubitemid 37522197)
59. Robinson JC, Challa VR, Jones DS, Kelly DL Jr. Pericytosis and edema generation: a unique clinicopathologica variant of meningioma. Neurosurgery 1996; 39: 700-706.
60. Rouget C. Sur la contractilite des capillaires sanguins. C R Acad Sci (Paris) 1879; 88: 916.
61. Schlingemann RO, Rietveld FJ, De Waal RM, Ferrone S, Ruiter DJ. Expression of the high molecular weight melanoma-associated antigen by pericytes during angiogenesis in tumors and in healing wounds. Am J Pathol 1990; 136: 1393-1405. (Pubitemid 20210338)
62. Semchenko VV, Stepanov SS, Savchenko A. Ultrastructural manifestation of brain edema-swelling in neurooncologic patients. Zh Vopr Neirokhir Im N N Burdenko 1984; 1: 16-20. (Pubitemid 14158582)
63. Shi X. Cochlear pericyte responses to acoustic trauma and the involvement of hypoxia-inducible factor-1alpha and vascular endothelial growth factor. Am J Pathol 2009; 174: 1692-1704.
64. Szpak GM, Lewandowska E, Wierzba-Bobrowicz T, Bertrand E, Pasennik E, Mendel T, Stȩpień T, Leszczyńska A, Rafałowska J. Small cerebral vessel disease in familial amyloid and non-amyloid angiopathies: FAD-PS-1 (P117L) mutation and CADASIL. Immunohistochemical and ultrastructural studies. Folia Neuropathol 2007; 45: 192-204. (Pubitemid 351149045)
65. Stensaas LJ. Pericytes and perivascular microglial cells in the basal forebrain of the neonatal rabbit. Cell Tissue Res 1975; 158: 517-541.
66. Tagami M, Nara Y, Kubota A, Fujino H, Yamori Y. Ultrastructural changes in cerebral pericytes and astrocytes of stroke-prone spontaneously hypertensive rats. Stroke 1990; 21: 1064-1071. (Pubitemid 20218172)
67. Tagami M, Kubota A, Nara Y, Yamori Y. Detailed disease processes of cerebral pericytes and astrocytes in stroke-prone SHR rats. Clin Exp Hypertens A 1991; 13: 1069-1075.
68. Thomas WE. Brain macrophages: on the role of pericytes and perivascular cells. Brain Res Brain Res Rev 1999; 31: 41-57.
69. Torack RM. Ultrastructure of capillary reaction to brain tumors. Arch Neurol 1961; 5: 86-98.
70. van der Avoort IA, van der Laak JA, Otte-Höller I, van de Nieuwenhof HP, Massuger LF, De Hullu JA, van Kempen LC. The prognostic value of blood and lymph vessel parameters in lichen sclerosus for vulvar squamous cell carcinoma development: an immunohistochemical and electron microscopy study. Am J Obstet Gynecol 2010; 203: 167-168.
71. van Deurs B. Observations on the blood-brain barrier in hypertensive with particular references to phagocytic pericytes. J Ultrastruct Res 1976; 56: 65-77.
72. Verbeek MM, De Waal RM, Schipper JJ, van Nostrand WE. Rapid degeneration of cultured humanbrain pericytes by amyloid beta protein. J Neurochem 1997; 68: 1135-1141. (Pubitemid 27086218)
73. Verbeek MM, van Nostrand WE, Otte-Holler I, Wesseling P, De Waaj RM. Amyloid-beta-induced degeneration of human brain pericytes dependent on the apolipoprotein E genotype. Ann NY Acad Sci 2000; 903: 187-199. (Pubitemid 30251558)
74. Wegiel J, Wisniewski HM. Tubuloreticular structures in microglial cells, pericytes and endothelial cells in Alzheimer's disease. Acta Neuropathol 1992; 83: 653-658.
75. Yamagishi S, Imaizumi T. Pericyte biology and diseases. Int J Tissue React 2005; 2: 125-135. (Pubitemid 41723729)