Skip to main content
SpringerLink
Log in

Ultrastructure of cerebellar capillary hemangioblastoma

IV. Pericytes and their relationship to endothelial cells

  • Original Works
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Summary

Electron microscopy and computerized morphometric techniques were employed to examine pericyte ultrastructure and to assess quantitatively their relationship to endothelial cells in five cases of cerebellar capillary hemangioblastoma. A total of 97 cross-sectioned capillary profiles were studied. Pericyte coverage of capillary ranged from 30.2% to 97.3% with a mean value of 68.7%, which is higher as compared with the available data from the cerebral cortex, skeletal and cardiac muscle, and pulmonary capillaries. The higher pericyte coverage of capillary suggests that pericyte is an active component of cerebellar capillary hemangioblastoma and may have a close functional relationship to endothelial cells. Pericytes contained bundles of parallel microfilaments along the adluminal side and in the terminal processes, and exhibited an intimate “peg-and-socket” relationship with endothelial cells, suggesting a contractile function of pericytes and their possible role in regulating capillary lumina and focal blood flow. The finding of abundant micropinocytic vesicles along the abluminal side of the cytoplasmic membrane indicates an active metabolic exchange between pericytes and the interstitium. It is possible that in cerebellar hemangioblastoma pericytes may act as a mechanical and metabolic monitor barrier for endothelial cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Allsopp G, Gamble HJ (1979) An electron-microscopic study of the pericytes of the developing capillaries in human fetal brain and muscle. J Anat 128:155–168

    Google Scholar 

  2. Ausprun KDH, Folkman J (1977) Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res 14:53–65

    Google Scholar 

  3. Azizkhan RG, Azizkhan JC, Zetter BR (1980) Mast cell heparin stimulates migration of capillary endothelial cells in vitro. J Exp Med 152:931–944

    Google Scholar 

  4. Baron M, Gallego A (1972) The relationship of the microglia with the pericytes in the cat cerebral cortex. Z Zellforsch 128:42–57

    Google Scholar 

  5. Bruns RR, Palade GE (1968) Studies on blood capillaries. I. General organization of blood capillaries in muscle. J Cell Biol 37:244–276

    Google Scholar 

  6. Burger PC, Klintworth GK (1981) Autoradiographic study of corneal neovascularization induced by chemical cautery. Lab Invest 45:328–335

    Google Scholar 

  7. Cancilla PA, Baker RN, Pollock PS, Frommes SP (1972) The reaction of pericytes of the central nervous system to exogenous protein. Lab Invest 26:376–383

    Google Scholar 

  8. Castejon OJ (1984) Submicroscopic changes of cortical capillary pericytes in human perifocal brain edema. J Submicrosc Cytol 16:601–618

    Google Scholar 

  9. 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

    Google Scholar 

  10. Cervos-Navarro J (1971) Elektronenmikroskopie der Hämangioblastome des ZNS und der angioblastischen Meningiome. Acta Neuropathol (Berl) 19:184–207

    Google Scholar 

  11. Chaudhry AP, Montes M, Cohn GA (1978) Ultrastructure of cerebellar hemangioblastoma. Cancer 42:1834–1850

    Google Scholar 

  12. Cliff WJ (1976) The extra-endothelial cells of blood vessel walls. In: Cliff WJ (ed) Blood vessels. Cambridge University Press, Cambridge, pp 68–96

    Google Scholar 

  13. Cohen MP, Frank RN, Khalifa AA (1980) Collagen production by cultured retinal capillary pericytes. Invest Ophthalmol Vis Sci 19:90–94

    Google Scholar 

  14. Cotran RS, Majno G (1964) A light- and electron-microscopic analysis of vascular injury. Ann NY Acad Sci 116:750–763

    Google Scholar 

  15. Courtoy PJ, Boyles J (1983) Fibronectin in the microvasculature: Localization in the pericyte-endothelium interstitium. J Ultrastruct Res 83:258–273

    Google Scholar 

  16. Crocker DJ, Murad TM, Geer JC (1970) Role of the pericyte in wound healing. An ultrastructural study. Exp Mol Pathol 13:51–65

    Google Scholar 

  17. Dodson RE (1973) Electron microscopy of microvascular pericytes in the brain. Cytobios 1:183–188

    Google Scholar 

  18. Dodson RE, Tagashira Y, Chu WFL (1976) Acute pericyte response to cerebral ischemia. J Neurol Sci 29:9–16

    Google Scholar 

  19. Donahue S, Pappas GD (1961) The fine structure of capillaries in the cerebral cortex of the rat at various stages of development. Am J Anat 108:331–347

    Google Scholar 

  20. Drenckhahn D, Groschel-Stewart U, Stumpf B (1980) Besitzen Endothelzellen und Perizyten in verschiedenen Abschnitten der terminalen Strombahn und in verschiedenen Organen unterschiedliche Mengen und Typen von Myosin? Arbeitstag Würzburg 2:85

    Google Scholar 

  21. Epling GP (1966) Electron-microscopic observations of pericytes of small blood vessels in the lungs and hearts of normal cattle and swine. Anat Rec 155:513–517

    Google Scholar 

  22. Folkman J, Taylor S, Spillberg C (1983) The role of heparin in angiogenesis. In: Nugent J, O'Connor M (eds) Development of the vascular system. Ciba Foundation Symposium 100. Pitman, London, pp 132–149

    Google Scholar 

  23. Forbes MS, Rennels ML, Nelson E (1977) Ultrastructure of pericytes in mouse heart. Am J Anat 149:47–70

    Google Scholar 

  24. Hauw JJ, Berger B, Escourolle R (1975) Electron-microscopic study of the developing capillaries of human brain. Acta Neuropathol (Berl) 31:229–242

    Google Scholar 

  25. Ho KL (1984) Ultrastructure of cerebellar capillary hemangioblastoma. I. Weibel-Palade bodies and stromal cell histogenesis. J Neuropathol Exp Neurol 43:592–608

    Google Scholar 

  26. Ho KL (1984) Ultrastructure of cerebellar capillary hemangioblastoma. II. Mast cells and angiogenesis. Acta Neuropathol (Berl) 64:308–318

    Google Scholar 

  27. Ho KL (1985) Ultrastructure of cerebellar capillary hemangioblastoma. III. Crystalloid bodies in endothelial cells. Acta Neuropathol (Berl) 66:117–126

    Google Scholar 

  28. 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

    Google Scholar 

  29. Kawamura J, Garcia JH, Kamijyo Y (1973) Cerebellar hemangioblastomas. Histogenesis of stromal cells. Cancer 31:1528–1540

    Google Scholar 

  30. Kessler DA, Langer RS, Pless NA, Folkman J (1976) Mast cells and tumor angiogenesis. Int J Cancer 18:703–709

    Google Scholar 

  31. Kristensson K, Olsson Y (1973) Accumulation of protein tracers in pericytes of the central nervous system following systemic injection in immature mice. Acta Neurol Scand 49:189–194

    Google Scholar 

  32. Lafarga M, Palacios G (1975) Ultrastructural study of pericytes in the rat supraoptic nucleus. J Anat 120:433–438

    Google Scholar 

  33. LeBeux YJ, Willemot J (1978) Actin and myosin-like filaments in rat brain pericytes. Anat Rec 190:811–826

    Google Scholar 

  34. LeBeux YJ, Willemot J (1978) Actin-like filaments in the endothelial cells of adult rat brain capillaries. Exp Neurol 58:446–454

    Google Scholar 

  35. Leeson TS (1979) Rat retinal blood vessels. Can J Ophthalmol 14:21–28

    Google Scholar 

  36. Majno G, Palade GE (1961) Studies in inflammation. I. The effect of histamine and serotonin on vascular permeability: An electron-microscopic study. J Biophys Biochem Cytol 2:571–605

    Google Scholar 

  37. Majno G (1965) Ultrastructure of the vascular membrane, In: Hamilton WF, Dow P (eds) Handbook of physiology, sect 2, vol 3. Circulation. Amer Physiol Soc, Washington, DC, pp 2293–2375

    Google Scholar 

  38. Mato M, Ookawara S, Kurihora K (1980) Uptake of exogenous substances and marked infoldings of the fluorescent granular pericytes in cerebral fine vessels. Am J Anat 157:329–332

    Google Scholar 

  39. Mazant R, Franzini-Armstrong C (1982) Scanning electron microscopy of pericytes in rat red muscle. Microvasc Res 23:361–369

    Google Scholar 

  40. Meyrick B, Reid L (1978) The effect of continued hypoxia on rat pulmonary arterial circulation. An ultrastructural study. Lab Invest 38:188–200

    Google Scholar 

  41. Moffat DB (1967) The fine structure of the blood vessels of the renal medulla with particular reference to the control of the medullary circulation. J Ultrastruct Res 19:532–545

    Google Scholar 

  42. Movat HZ, Fernando NVP (1964) The fine structure of the terminal vascular bed. IV. The venules and their perivascular cells (pericytes, adventitial cells). Exp Mol Pathol 3:98–114

    Google Scholar 

  43. Povlishock Jt, Martinez AJ, Moossy J (1977) The fine structure of blood vessels of the telencephalic germinal matrix in the human fetus. Am J Anat 149:439–452

    Google Scholar 

  44. Rhodin J (1968) Ultrastructure of mammalian venous capillaries, venules and small collecting veins. Ultrastruct Res 25:452–500

    Google Scholar 

  45. Rouget C (1873) Memoire sur le developpement, la structure et les propriets physiologiques des capillaries sanguins et lymphatiques. Arch Physiol Norm Pathol 5:603–663

    Google Scholar 

  46. Shakib M, De Oliveria F, (1966) Studies on developing retinal vessels. X. Formation of the basement membrane and differentiation of intramural pericytes. Br J Ophthalmol 50:124–133

    Google Scholar 

  47. Shalley MM, Cavallo T, Cotran RS (1977) Endothelial proliferation in inflammation. I. Autoradiographic studies following thermal injury to the skin of normal rats. Am J Pathol 89:277–296

    Google Scholar 

  48. Sims DE, Westfall JA (1983) Analysis of relationships between pericytes and gas exchange capillaries in neonatal and mature bovine lungs. Microvasc Res 25:333–342

    Google Scholar 

  49. Spence AM, Rubinstein LJ (1975) Cerebellar capillary hemangioblastoma — its histogenesis studied by organ culture and electron microscopy. Cancer 35:326–341

    Google Scholar 

  50. Spitznas M (1974) The fine structure of the chorioretinal border tissues of the adult human eye. Adv Ophthalmol 28:78–174

    Google Scholar 

  51. Stensaas LJ (1975) Pericytes and perivascular microglial cells in the basal forebrain of the neonatal rabbit. Cell Tissue Res 158:517–541

    Google Scholar 

  52. Tilton RG, Kilo C, Williamson JR (1979) Pericyte-endothelial relationships in cardiac and skeletal muscle capillaries. Microvasc Res 18:325–335

    Google Scholar 

  53. Tilton RG, Kilo C, Williamson JR, March DW (1979) Differences in pericytes contractile function in rat cardiac and skeletal muscle microvasculatures. Microvasc Res 18:336–352

    Google Scholar 

  54. Van Deur B (1976) Observations on the blood-brain barrier in hypertension with particular reference to phagocytic pericytes. J Ultrastruct Res 56:65–77

    Google Scholar 

  55. Wallow IH, Burnside B (1980) Actin filaments in retinal pericytes and endothelial cells. Invest Ophtalmol Vis Sci 19:1433–1441

    Google Scholar 

  56. Weibel ER (1974) On pericytes, particularly their existence on lung capillaries. Microvasc Res: 218–235

  57. Williamson JR, Tilton RG, Kilo C, Simon Y (1980) Immunofluorescent imaging of capillaries and pericytes in human skeletal muscle and retina. Microvasc Res 20:233–241

    Google Scholar 

  58. Zimmermann KW (1923) Der feinere Bau der Blutcapillaren. Z Anat Entwicklungsgesch 68:3–109

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dept. of Pathology, Henry Ford Hospital, 2799 West Grand Boulevard, 48202, Detroit, MI, USA

    K. L. Ho

Authors
  1. K. L. Ho
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by Henry Ford Hospital research grant R36274

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ho, K.L. Ultrastructure of cerebellar capillary hemangioblastoma. Acta Neuropathol 67, 254–264 (1985). https://doi.org/10.1007/BF00687810

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00687810

Key words

Search

Navigation