BRAIN CAPILLARIES: HETEROGENEITY IS THE WORD OF ORDER

BRAIN CAPILLARIES: HETEROGENEITY IS THE WORD OF ORDER

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Title:	BRAIN CAPILLARIES: HETEROGENEITY IS THE WORD OF ORDER
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Article_Title:	BRAIN CAPILLARIES: HETEROGENEITY IS THE WORD OF ORDER
Authors:	Maria SUCIU1*, Aurel ARDELEAN1, Anca HERMENEAN1
Affiliation:	1Institute of Life Sciences, Western University “Vasile Goldis” of Arad, Arad, Romania
Abstract:	Capillaries are the smallest vessels of the circulatory tree, having similar functions for the entire body, but also functions that are specific for a certain type of organ or tissue. Capillaries are composed of endothelial cells, pericytes that assist them and a basal membrane that envelopes them. Through this review we wanted to emphasize the fact that capillaries are a generic name for a very malleable structure that is found everywhere in the body. We focused on differences that appear generally between capillaries in the body and specifically in the brain, and we went further to search if there are differences within a single capillary network that connects the arterial and venous sides. There are morphological variations of microvessels within the brain and molecular differences within the same capillary tube, differences that appertain to their arterial or venous characteristics.
Keywords:	capillary, brain, difference, blood-brain barrier, histology.
References:	Eichmann A, Yuan L, Moyon D, Lenoble F, Pardanaud L, Breant C. (2005) Vascular development: from precursor cells to branched arterial and venous networks. Int J Dev Biol., 49 (2-3), pp:259-267. Pavelka M, Roth J. (2010) Endothelia. In: Functional Ultrastructure, Atlas of Tissue Biology and Pathology, 2nd Ed, chap. 9, pp:254-261, Edited by M. Pavelka and J. Roth, SpringerWienNewYork. Bechmann I, Galea I, Perry VH. (2007) What is the blood-brain barrier (not)? Trends Immunol., 28(1) pp: 5–11. Abbott NJ, Rönnbäck L, Hansson E. (2006) Astrocyte–endothelial interactions at the blood–brain barrier. Nature Reviews, Neuroscience, 7, pp: 41-53. Hawkins BT, Davis TP. (2005) The blood–brain barrier. Neurovascular unit in health and disease. Pharmacol. Rev., 57, pp: 173–185. Saunders NR, Liddelow SA, Dziegielewska KM. (2012) Barrier mechanisms in the developing brain. Front Pharmacol., 3, p: 46. Bartanusz V, Jezova D, Alajajian B, Digicaylioglu M. (2011) The blood-spinal cord barrier: morphology and clinical implications. Ann. Neurol., 70(2) pp: 194-206. Runkle EA, Antonetti DA. (2011) The Blood-Retinal Barrier: Structure and Functional Significance. In The Blood-Brain and Other Neural Barriers, Reviews and Protocols, Methods in Molecular Biology, vol. 686, p: 144 – 148, edited by S., Nag, Springer Science+Business Media, Toronto. Weerasuriya A, Mizisin AP. (2011) The Blood-Nerve Barrier: Structure and Functional Significance. In The Blood-Brain and Other Neural Barriers, Reviews and Protocols, Methods in Molecular Biology, vol. 686, p: 149 – 175, Edited by S., Nag, Springer Science+Business Media, Toronto. Engelhardt B. (2008) The blood-central nervous system barriers actively control immune cell entry into the central nervous system. Curr. Pharm. Des., 14(16), pp: 1555-1565. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP. (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest., 105(1), pp: 71–77. Farrall AJ, Wardlaw JM. (2009) Blood–brain barrier: Ageing and microvascular disease – systematic review and meta-analysis. J. Neurobiol. Aging, 30(3) pp: 337–352. Kalinowski L, Dobrucki IT, Malinski T. (2004) Race-specific differences in endothelial function: predisposition of African Americans to vascular diseases. Circulation., 109 (21), pp: 2511-2517. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, Pober JS, Wick TM, Konkle BA, Schwartz BS, Barnathan ES, McCrae KR, Hug BA, Schmidt AM, Stern DM. (1998) Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood., 91(10), 3527-3561. Ribatti D, Crivellato E, (2012) Vascular Development. In: Inflammatory Diseases of Blood Vessels, 2nd Ed., pp: 3-7, Edited by G. Hoffman, C.M. Weyand, C.A. Langford, and J.J. Goronzy, Wiley Blackwell, New Delhi. Roberts WG, Palade GE. (1997) Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res. 57(4), pp:765-72. Roberts WG, Palade GE. (1995) Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci. 108( Pt 6), pp:2369-79. Casley-Smith JR. (1971) Endothelial fenestrae in intestinal villi: differences between the arterial and venous ends of the capillaries. Microvasc Res., 3(1), pp: 49-68. Braverman IM, Yen A. (1977) Ultrastructure of the human dermal microcirculation. II. The capillary loops of the dermal papillae. J Invest Dermatol., 68(1) 44-52. (a) Braverman IM, Yen A. (1977) Ultrastructure of the capillary loops in the dermal papillae of psoriasis. J Invest Dermatol., 68(1) 53-60. (b) Yen A, Braverman IM. (1976) Ultrastructure of the human dermal microcirculation: the horizontal plexus of the papillary dermis. J Invest Dermatol., 66(3), pp:131-42. Pusztaszeri MP, Seelentag W, Bosman FT. (2006) Immunohistochemical expression of endothelial markers CD31, CD34, von Willebrand factor, and Fli-1 in normal human tissues. J Histochem Cytochem., 54(4), pp: 385-395. Watzman HM, Kurth CD, Montenegro LM, Rome J, Steven JM, Nicolson SC. (2000) Arterial and venous contributions to near-infrared cerebral oximetry. Anesthesiology, 93(4), pp: 947-953. Muller AM, Hermanns MI, Skrzynski C, Nesslinger M, Muller KM, Kirppatrick J. (2002) Expression of the endothelial markers PECAM-1, VWf and CD34 in vivo and in vitro. Exp. Mol. Pathol., 72, pp: 221–229. Kawanami O, Jin E, Ghazizadeh M, Fujiwara M, Jiang L, Nagashima M, Shimizu H, Takemura T, Ohaki Y, Arai S, Gomibuchi M, Takeda K, Yu ZX, Ferrans VJ. (2000) Heterogeneous distribution of thrombomodulin.and von Willebrand factor in endothelial cells in the human pulmonary microvessels. J. Nippon Med. Sch., 67, pp: 118–125. Hewett PW, Nishi K, Daft EL, Clifford Murray J. (2001) Selective expression of erg isoforms in human endothelial cells. Int. J. Biochem. Cell Biol., 33, pp: 347–355. le Noble F, Moyon D, Pardanaud L, Yuan L, Djonov V, Matthijsen R, Bréant C, Fleury V, Eichmann A. (2004) Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development., 131(2), pp: 361-375. Gale NW, Baluk P, Pan L, Kwan M, Holash J, DeChiara TM, McDonald DM, Yancopoulos GD. (2001) Ephrin-B2 selectively marks arterial vessels and neovascularization sites in the adult, with expression in both endothelial and smooth-muscle cells. Dev. Biol., 230, pp: 151–160. Shin D, Garcia-Cardena G, Hayashi S, Gerety S, Asahara T, Stavrakis G, Isner J, Folkman J, Gimbrone MAJr., Anderson DJ. (2001) Expression of ephrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev Biol., 230(2), pp: 139-50. Wang HU, Chen ZF, Anderson DJ. (1998) Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell, 93(5), pp: 741-753. Red-Horse K, Ueno H, Weissman IL, Krasnow MA. (2010) Coronary arteries form by developmental reprogramming of venous cells. Nature, 464 (7288), pp: 549-553. Bianchi C, Sellke FW, Del Vecchio RL, Tonks NK, Neel BG. (1999) Receptor-type protein-tyrosine phosphatase mu is expressed in specific vascular endothelial beds in vivo. Exp Cell Res., 248(1), pp: 329-38. Koyama T, Xie Z, Gao M, Suzuki J, Batra S. (1998) Adaptive changes in the capillary network in the left ventricle of the rat heart. Jap. J. Physiol., 48, pp: 229 –241. Kowal RC, Richardson JA, Miano JM, Olson EN. (1999) EVEC, a novel epidermal growth factor-like repeat-containing protein upregulated in embryonic and diseased adult vasculature. Circ. Res., 84, pp: 1166 –1176. Nakamura T, Ruiz-Lozano P, Lindner V, Yabe D, Taniwaki M, Furukawa Y, Kobuke K, Tashiro K, Lu Z, Andon NL, Schaub R, Matsumori A, Sasayama S, Chien KR, Honjo T. (1999) DANCE, a novel secreted RGD protein expressed in developing, atherosclerotic, and balloon-injured arteries. J. Biol. Chem., 274 (22476 –22483). Nakagawa O, Nakagawa M, Richardson JA, Olson EN, Srivastava D. (1999) HRT1, HRT2, and HRT3:A new subclass of bHLH transcription factors marking specific cardiac, somitic and pharyngeal arch segments. Dev. Biol., 216 pp: 72– 84. Fang J, Li X, Smiley E, Francke U, Mecham RP, Bonadio J. (1997) Mouse latent TGF-b binding protein-2: Molecular cloning and developmental expression. Biochim. Biophys. Acta, 1354, pp: 219 –230. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. (1997) A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1a regulates the VEGF expression and is potentially involved in lung and vascular development. Proc. Natl. Acad. Sci. USA, 94, pp: 4273– 4278. Flamme I, Frohlich T, Reutern M, Kappel A, Damert A, Risau W. (1997) HRF, a putative basic helix-loop-helix-PAS domain transcription factor is closely related to hypoxia-inducible factor-1 a and developmentally expressed in blood vessels. Mech. Dev., 63, pp: 51– 60. Baluk P. McDonald DM. (2008) Markers for microscopic imaging of lymphangiogenesis and angiogenesis. Ann N Y Acad Sci., 1131, pp: 1-12. Clark ER, Clark EL. (1932) Observations on living preformed blood vessels as seen in transparent chamber inserted into the rabbit’s ear. Am. J. Anat., 49, pp: 441-477.
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Correspondence:	80-86, Liviu Rebreanu Str., Institute of Life Sciences, Western University “Vasile Goldis” of Arad, Arad, Romania

	Read full article
Article Title:	BRAIN CAPILLARIES: HETEROGENEITY IS THE WORD OF ORDER
Authors:	Maria SUCIU1*, Aurel ARDELEAN1, Anca HERMENEAN1
Affiliation:	1Institute of Life Sciences, Western University “Vasile Goldis” of Arad, Arad, Romania
Abstract:	Capillaries are the smallest vessels of the circulatory tree, having similar functions for the entire body, but also functions that are specific for a certain type of organ or tissue. Capillaries are composed of endothelial cells, pericytes that assist them and a basal membrane that envelopes them. Through this review we wanted to emphasize the fact that capillaries are a generic name for a very malleable structure that is found everywhere in the body. We focused on differences that appear generally between capillaries in the body and specifically in the brain, and we went further to search if there are differences within a single capillary network that connects the arterial and venous sides. There are morphological variations of microvessels within the brain and molecular differences within the same capillary tube, differences that appertain to their arterial or venous characteristics.
Keywords:	capillary, brain, difference, blood-brain barrier, histology.
References:	Eichmann A, Yuan L, Moyon D, Lenoble F, Pardanaud L, Breant C. (2005) Vascular development: from precursor cells to branched arterial and venous networks. Int J Dev Biol., 49 (2-3), pp:259-267. Pavelka M, Roth J. (2010) Endothelia. In: Functional Ultrastructure, Atlas of Tissue Biology and Pathology, 2nd Ed, chap. 9, pp:254-261, Edited by M. Pavelka and J. Roth, SpringerWienNewYork. Bechmann I, Galea I, Perry VH. (2007) What is the blood-brain barrier (not)? Trends Immunol., 28(1) pp: 5–11. Abbott NJ, Rönnbäck L, Hansson E. (2006) Astrocyte–endothelial interactions at the blood–brain barrier. Nature Reviews, Neuroscience, 7, pp: 41-53. Hawkins BT, Davis TP. (2005) The blood–brain barrier. Neurovascular unit in health and disease. Pharmacol. Rev., 57, pp: 173–185. Saunders NR, Liddelow SA, Dziegielewska KM. (2012) Barrier mechanisms in the developing brain. Front Pharmacol., 3, p: 46. Bartanusz V, Jezova D, Alajajian B, Digicaylioglu M. (2011) The blood-spinal cord barrier: morphology and clinical implications. Ann. Neurol., 70(2) pp: 194-206. Runkle EA, Antonetti DA. (2011) The Blood-Retinal Barrier: Structure and Functional Significance. In The Blood-Brain and Other Neural Barriers, Reviews and Protocols, Methods in Molecular Biology, vol. 686, p: 144 – 148, edited by S., Nag, Springer Science+Business Media, Toronto. Weerasuriya A, Mizisin AP. (2011) The Blood-Nerve Barrier: Structure and Functional Significance. In The Blood-Brain and Other Neural Barriers, Reviews and Protocols, Methods in Molecular Biology, vol. 686, p: 149 – 175, Edited by S., Nag, Springer Science+Business Media, Toronto. Engelhardt B. (2008) The blood-central nervous system barriers actively control immune cell entry into the central nervous system. Curr. Pharm. Des., 14(16), pp: 1555-1565. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP. (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest., 105(1), pp: 71–77. Farrall AJ, Wardlaw JM. (2009) Blood–brain barrier: Ageing and microvascular disease – systematic review and meta-analysis. J. Neurobiol. Aging, 30(3) pp: 337–352. Kalinowski L, Dobrucki IT, Malinski T. (2004) Race-specific differences in endothelial function: predisposition of African Americans to vascular diseases. Circulation., 109 (21), pp: 2511-2517. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, Pober JS, Wick TM, Konkle BA, Schwartz BS, Barnathan ES, McCrae KR, Hug BA, Schmidt AM, Stern DM. (1998) Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood., 91(10), 3527-3561. Ribatti D, Crivellato E, (2012) Vascular Development. In: Inflammatory Diseases of Blood Vessels, 2nd Ed., pp: 3-7, Edited by G. Hoffman, C.M. Weyand, C.A. Langford, and J.J. Goronzy, Wiley Blackwell, New Delhi. Roberts WG, Palade GE. (1997) Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res. 57(4), pp:765-72. Roberts WG, Palade GE. (1995) Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci. 108( Pt 6), pp:2369-79. Casley-Smith JR. (1971) Endothelial fenestrae in intestinal villi: differences between the arterial and venous ends of the capillaries. Microvasc Res., 3(1), pp: 49-68. Braverman IM, Yen A. (1977) Ultrastructure of the human dermal microcirculation. II. The capillary loops of the dermal papillae. J Invest Dermatol., 68(1) 44-52. (a) Braverman IM, Yen A. (1977) Ultrastructure of the capillary loops in the dermal papillae of psoriasis. J Invest Dermatol., 68(1) 53-60. (b) Yen A, Braverman IM. (1976) Ultrastructure of the human dermal microcirculation: the horizontal plexus of the papillary dermis. J Invest Dermatol., 66(3), pp:131-42. Pusztaszeri MP, Seelentag W, Bosman FT. (2006) Immunohistochemical expression of endothelial markers CD31, CD34, von Willebrand factor, and Fli-1 in normal human tissues. J Histochem Cytochem., 54(4), pp: 385-395. Watzman HM, Kurth CD, Montenegro LM, Rome J, Steven JM, Nicolson SC. (2000) Arterial and venous contributions to near-infrared cerebral oximetry. Anesthesiology, 93(4), pp: 947-953. Muller AM, Hermanns MI, Skrzynski C, Nesslinger M, Muller KM, Kirppatrick J. (2002) Expression of the endothelial markers PECAM-1, VWf and CD34 in vivo and in vitro. Exp. Mol. Pathol., 72, pp: 221–229. Kawanami O, Jin E, Ghazizadeh M, Fujiwara M, Jiang L, Nagashima M, Shimizu H, Takemura T, Ohaki Y, Arai S, Gomibuchi M, Takeda K, Yu ZX, Ferrans VJ. (2000) Heterogeneous distribution of thrombomodulin.and von Willebrand factor in endothelial cells in the human pulmonary microvessels. J. Nippon Med. Sch., 67, pp: 118–125. Hewett PW, Nishi K, Daft EL, Clifford Murray J. (2001) Selective expression of erg isoforms in human endothelial cells. Int. J. Biochem. Cell Biol., 33, pp: 347–355. le Noble F, Moyon D, Pardanaud L, Yuan L, Djonov V, Matthijsen R, Bréant C, Fleury V, Eichmann A. (2004) Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development., 131(2), pp: 361-375. Gale NW, Baluk P, Pan L, Kwan M, Holash J, DeChiara TM, McDonald DM, Yancopoulos GD. (2001) Ephrin-B2 selectively marks arterial vessels and neovascularization sites in the adult, with expression in both endothelial and smooth-muscle cells. Dev. Biol., 230, pp: 151–160. Shin D, Garcia-Cardena G, Hayashi S, Gerety S, Asahara T, Stavrakis G, Isner J, Folkman J, Gimbrone MAJr., Anderson DJ. (2001) Expression of ephrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev Biol., 230(2), pp: 139-50. Wang HU, Chen ZF, Anderson DJ. (1998) Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell, 93(5), pp: 741-753. Red-Horse K, Ueno H, Weissman IL, Krasnow MA. (2010) Coronary arteries form by developmental reprogramming of venous cells. Nature, 464 (7288), pp: 549-553. Bianchi C, Sellke FW, Del Vecchio RL, Tonks NK, Neel BG. (1999) Receptor-type protein-tyrosine phosphatase mu is expressed in specific vascular endothelial beds in vivo. Exp Cell Res., 248(1), pp: 329-38. Koyama T, Xie Z, Gao M, Suzuki J, Batra S. (1998) Adaptive changes in the capillary network in the left ventricle of the rat heart. Jap. J. Physiol., 48, pp: 229 –241. Kowal RC, Richardson JA, Miano JM, Olson EN. (1999) EVEC, a novel epidermal growth factor-like repeat-containing protein upregulated in embryonic and diseased adult vasculature. Circ. Res., 84, pp: 1166 –1176. Nakamura T, Ruiz-Lozano P, Lindner V, Yabe D, Taniwaki M, Furukawa Y, Kobuke K, Tashiro K, Lu Z, Andon NL, Schaub R, Matsumori A, Sasayama S, Chien KR, Honjo T. (1999) DANCE, a novel secreted RGD protein expressed in developing, atherosclerotic, and balloon-injured arteries. J. Biol. Chem., 274 (22476 –22483). Nakagawa O, Nakagawa M, Richardson JA, Olson EN, Srivastava D. (1999) HRT1, HRT2, and HRT3:A new subclass of bHLH transcription factors marking specific cardiac, somitic and pharyngeal arch segments. Dev. Biol., 216 pp: 72– 84. Fang J, Li X, Smiley E, Francke U, Mecham RP, Bonadio J. (1997) Mouse latent TGF-b binding protein-2: Molecular cloning and developmental expression. Biochim. Biophys. Acta, 1354, pp: 219 –230. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. (1997) A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1a regulates the VEGF expression and is potentially involved in lung and vascular development. Proc. Natl. Acad. Sci. USA, 94, pp: 4273– 4278. Flamme I, Frohlich T, Reutern M, Kappel A, Damert A, Risau W. (1997) HRF, a putative basic helix-loop-helix-PAS domain transcription factor is closely related to hypoxia-inducible factor-1 a and developmentally expressed in blood vessels. Mech. Dev., 63, pp: 51– 60. Baluk P. McDonald DM. (2008) Markers for microscopic imaging of lymphangiogenesis and angiogenesis. Ann N Y Acad Sci., 1131, pp: 1-12. Clark ER, Clark EL. (1932) Observations on living preformed blood vessels as seen in transparent chamber inserted into the rabbit’s ear. Am. J. Anat., 49, pp: 441-477.
*Correspondence:	80-86, Liviu Rebreanu Str., Institute of Life Sciences, Western University “Vasile Goldis” of Arad, Arad, Romania

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