Skip to main content
Top
Published in: Surgical and Radiologic Anatomy 10/2011

01-12-2011 | Original Article

Cd34-positive developing vessels and other structures in human fetuses: an immunohistochemical study

Authors: Shin-ichi Abe, Masashi Suzuki, Kwang Ho Cho, Gen Murakami, Baik Hwan Cho, Yoshinobu Ide

Published in: Surgical and Radiologic Anatomy | Issue 10/2011

Login to get access

Abstract

CD34 is a well-known marker of progenitor cells of blood vessels and stromal tissues. Thus, CD34-positive cells have recently been used clinically in the field of vascular and orthopedic biotechnology because of their capacity to assist regeneration of injured tissues. However, to our knowledge, the in situ distribution of CD34-positive cells has not yet been described in the human fetus, with the exception of a few organs. In the present study, we conducted immunohistochemistry for CD34 using 12 human fetuses (9–15 weeks of gestation). CD34-positive structures showed a vessel-like appearance and were regularly arrayed in the viscera, nerves and lymph nodes, whereas in the body wall and extremities, they were distributed diffusely as fibrous tissues, such as the fascia and perimysium. The myocardium was also divided and bundled by CD34-positive fibrous tissues. In striated muscles, limited examples of CD34 expression were found in the tongue and extraocular muscles in which only vessels were positive. Lymphatic vessels were negative for CD34. In addition to their contribution to vascular development in any part of the body, CD34-positive mesenchymal tissues seem to play a critical role in the pattern formation of skeletal muscle, synovial tissue and other muscle/tendon-associated tissues in human fetuses.
Literature
1.
go back to reference Acarreguli MJ, England KM, Richman JT, Littig JL (2003) Characterization of CD34+ cells isolated from human fetal lung. Am J Physiol Lung Cell Mol Physiol 284:365–401 Acarreguli MJ, England KM, Richman JT, Littig JL (2003) Characterization of CD34+ cells isolated from human fetal lung. Am J Physiol Lung Cell Mol Physiol 284:365–401
2.
go back to reference Arisio R, Borissone M, Piccoli E, Panzica G (2002) Central nervous system microangioarchitecture in the human foetus. Adv Clin Path 6:125–129PubMed Arisio R, Borissone M, Piccoli E, Panzica G (2002) Central nervous system microangioarchitecture in the human foetus. Adv Clin Path 6:125–129PubMed
3.
go back to reference Christ B, Brand-Saberi B (2002) Limb muscle development. Int J Dev Biol 46:905–914PubMed Christ B, Brand-Saberi B (2002) Limb muscle development. Int J Dev Biol 46:905–914PubMed
4.
go back to reference Hanft VN, Shea CR, McNutt NS, Pullitzer D, Horenstein MG, Prieto VG (2000) Expression of CD34 in sclerotic (“plywood”) fibromas. Am J Dermatol 22:17–21CrossRef Hanft VN, Shea CR, McNutt NS, Pullitzer D, Horenstein MG, Prieto VG (2000) Expression of CD34 in sclerotic (“plywood”) fibromas. Am J Dermatol 22:17–21CrossRef
5.
go back to reference Hayashi S, Murakami G, Ohtsuka A, Itoh M, Nakano T, Fukuzawa Y (2008) Connective tissue configuration in the human liver hilar region with special reference to the liver capsule and vascular sheath. J Hepatobiliary Pancreat Surg 15:640–647PubMedCrossRef Hayashi S, Murakami G, Ohtsuka A, Itoh M, Nakano T, Fukuzawa Y (2008) Connective tissue configuration in the human liver hilar region with special reference to the liver capsule and vascular sheath. J Hepatobiliary Pancreat Surg 15:640–647PubMedCrossRef
6.
go back to reference Hermida-Gómez T, Fuentes-Boquete I, Gimeno-Lóngas MJ, Muińos-Lopez E, Diaz-Prado S, de Toro FJ, Blanco FJ (2011) Quantification of cells expressing mesenchymal stem cell markers in healthy and osteoarthritic synovial membrane. J Rheumatol 38(2):339–349 Hermida-Gómez T, Fuentes-Boquete I, Gimeno-Lóngas MJ, Muińos-Lopez E, Diaz-Prado S, de Toro FJ, Blanco FJ (2011) Quantification of cells expressing mesenchymal stem cell markers in healthy and osteoarthritic synovial membrane. J Rheumatol 38(2):339–349
7.
go back to reference Hughes S, Yang H, Chan-Ling T (2000) Vascularization of the human fetal retina: roles of vasculogenesis and angiogenesis. Invest Ophthalmol Vis Sci 41:1217–1228PubMed Hughes S, Yang H, Chan-Ling T (2000) Vascularization of the human fetal retina: roles of vasculogenesis and angiogenesis. Invest Ophthalmol Vis Sci 41:1217–1228PubMed
8.
go back to reference Invernici G, Ponti D, Corsini E, Cristini S, Frigerio S, Colombo A, Parati E, Alessandri G (2005) Human microvascular endothelial cells from different fetal organs demonstrate organ-specific CAM expression. Exp Cell Res 308:273–282PubMedCrossRef Invernici G, Ponti D, Corsini E, Cristini S, Frigerio S, Colombo A, Parati E, Alessandri G (2005) Human microvascular endothelial cells from different fetal organs demonstrate organ-specific CAM expression. Exp Cell Res 308:273–282PubMedCrossRef
9.
go back to reference Ishida K, Matsumoto T, Sasaki K, Mifune Y, Tei K, kubo S, Matsushita T, Takayama K, Akisue T, Tabata Y, Kurosaki M, Kuroda R (2010) Bone regeneration properties of granulocyte colony-stimulating factor via neovascularization and osteogenesis. Tissue Eng part A 16:3271–3284CrossRef Ishida K, Matsumoto T, Sasaki K, Mifune Y, Tei K, kubo S, Matsushita T, Takayama K, Akisue T, Tabata Y, Kurosaki M, Kuroda R (2010) Bone regeneration properties of granulocyte colony-stimulating factor via neovascularization and osteogenesis. Tissue Eng part A 16:3271–3284CrossRef
10.
go back to reference Jin ZW, Nakamura T, Yu HC, Kimura W, Murakami G, Cho BH (2010) Fetal anatomy of peripheral lymphatic vessels: a D2–40 immunohistochemical study using an 18-week human fetus (CRL 155 mm). J Anat 216:671–682PubMedCrossRef Jin ZW, Nakamura T, Yu HC, Kimura W, Murakami G, Cho BH (2010) Fetal anatomy of peripheral lymphatic vessels: a D2–40 immunohistochemical study using an 18-week human fetus (CRL 155 mm). J Anat 216:671–682PubMedCrossRef
11.
go back to reference Kohsla S, Westendorf JJ, Mödder UI (2010) Consice review: insights from normal bone remodeling and stem cell-based therapies for bone repair. Stem Cells 28:2124–2128CrossRef Kohsla S, Westendorf JJ, Mödder UI (2010) Consice review: insights from normal bone remodeling and stem cell-based therapies for bone repair. Stem Cells 28:2124–2128CrossRef
12.
go back to reference Kopher RA, Penchev VR, Islam MS, Hill KL, Khosla S, Kaufman DS (2010) Human embryonic stem cell-derived CD34+ cells function as MSC progenitor cells. Bone 47:718–728PubMedCrossRef Kopher RA, Penchev VR, Islam MS, Hill KL, Khosla S, Kaufman DS (2010) Human embryonic stem cell-derived CD34+ cells function as MSC progenitor cells. Bone 47:718–728PubMedCrossRef
13.
go back to reference Lee SY, Miwa M, Sakai Y, Kuroda R, Oe K, Niikura T, Matsumoto T, Fujioka H, Doita M, Kurosaka M (2008) Isolation and characterization of connective tissue progenitor cells derived from human fracture-induced hemarthrosis in vitro. J Orthop Res 26:190–1999PubMedCrossRef Lee SY, Miwa M, Sakai Y, Kuroda R, Oe K, Niikura T, Matsumoto T, Fujioka H, Doita M, Kurosaka M (2008) Isolation and characterization of connective tissue progenitor cells derived from human fracture-induced hemarthrosis in vitro. J Orthop Res 26:190–1999PubMedCrossRef
14.
go back to reference Lin CS, Xin ZC, Deng CH, Ning H, Lin G, Lue TF (2010) Defining adipose tissue-derived stem cells in tissue and in culture. Hitol Hitopathol 25:807–815 Lin CS, Xin ZC, Deng CH, Ning H, Lin G, Lue TF (2010) Defining adipose tissue-derived stem cells in tissue and in culture. Hitol Hitopathol 25:807–815
15.
go back to reference Miyake N, Hayashi S, Cho BH, Kawase T, Murakami G, Fujimiya M, Kitano H (2010) Fetal anatomy of the human carotid sheath and structures in and around it. Anat Rec 293:438–445CrossRef Miyake N, Hayashi S, Cho BH, Kawase T, Murakami G, Fujimiya M, Kitano H (2010) Fetal anatomy of the human carotid sheath and structures in and around it. Anat Rec 293:438–445CrossRef
16.
go back to reference Murakami G, Nakamura H (1991) Somites and the pattern formation of trunk muscles: a study in quail-chick chimera. Arch Histol Cytol 54:249–258PubMedCrossRef Murakami G, Nakamura H (1991) Somites and the pattern formation of trunk muscles: a study in quail-chick chimera. Arch Histol Cytol 54:249–258PubMedCrossRef
17.
go back to reference Nguyen VA, Fűrhapter C, Obexer P, Stössel H, Romani N, Sepp N (2009) Endothelial cells from cord CD133+ CD34+ progenitors share phenotypic, functional and gene expression profile similarities with lymphatics. J Cell Mol Med 13:522–534PubMedCrossRef Nguyen VA, Fűrhapter C, Obexer P, Stössel H, Romani N, Sepp N (2009) Endothelial cells from cord CD133+ CD34+ progenitors share phenotypic, functional and gene expression profile similarities with lymphatics. J Cell Mol Med 13:522–534PubMedCrossRef
18.
go back to reference Oberlin E, Tavian M, Blaszsek I, Pēault B (2002) Blood-forming potential of vascular endothelium in the human embryo. Development 129:4147–4157PubMed Oberlin E, Tavian M, Blaszsek I, Pēault B (2002) Blood-forming potential of vascular endothelium in the human embryo. Development 129:4147–4157PubMed
19.
go back to reference Pēault B, Tavian M (2003) Hematopoietic stem cell emergence in the human embryo and fetus. Ann NY Acad Sci 996:132–140PubMedCrossRef Pēault B, Tavian M (2003) Hematopoietic stem cell emergence in the human embryo and fetus. Ann NY Acad Sci 996:132–140PubMedCrossRef
20.
go back to reference Sakai Y, Matsukuma S (2002) CD34+ stromal cells and hyalinized vascular changes in the anal fibroepithelial polyps. Histopathology 41:230–235PubMedCrossRef Sakai Y, Matsukuma S (2002) CD34+ stromal cells and hyalinized vascular changes in the anal fibroepithelial polyps. Histopathology 41:230–235PubMedCrossRef
21.
go back to reference Shah KR, Wells MJ, Stetson CL (2010) CD34+ connective tissue nevi: are they unusual? J Am Acad Dermatol 62:719–720PubMedCrossRef Shah KR, Wells MJ, Stetson CL (2010) CD34+ connective tissue nevi: are they unusual? J Am Acad Dermatol 62:719–720PubMedCrossRef
22.
go back to reference Tavian M, Hallais MF, Peault B et al (1999) Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Development 126:793–803PubMed Tavian M, Hallais MF, Peault B et al (1999) Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Development 126:793–803PubMed
23.
go back to reference Tavian M, Pēault B (2005) Embryonic development of the human hematopoietic system. Int J Dev Biol 49:243–250PubMedCrossRef Tavian M, Pēault B (2005) Embryonic development of the human hematopoietic system. Int J Dev Biol 49:243–250PubMedCrossRef
24.
go back to reference Tavian M, Robin C, Coulombel L, Peault B (2001) The human embryo, but not its yolk sac, generates lympho-meyloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Immunity 15:487–495PubMedCrossRef Tavian M, Robin C, Coulombel L, Peault B (2001) The human embryo, but not its yolk sac, generates lympho-meyloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Immunity 15:487–495PubMedCrossRef
25.
go back to reference Waller EK, Huang S, Terstappen L (1995) Changes in the growth properties of CD34+, CD38- bone marrow progenitors during human fetal development. Blood 86:710–718PubMed Waller EK, Huang S, Terstappen L (1995) Changes in the growth properties of CD34+, CD38- bone marrow progenitors during human fetal development. Blood 86:710–718PubMed
26.
go back to reference Xu H, Edwards J, Banerji S, Prevo R, Jackson DG, Athanasou NA (2003) Distribution of lymohatic vessels in normal and arthritic human synovial tissues. Ann Rheum Dis 62:1227–1229PubMedCrossRef Xu H, Edwards J, Banerji S, Prevo R, Jackson DG, Athanasou NA (2003) Distribution of lymohatic vessels in normal and arthritic human synovial tissues. Ann Rheum Dis 62:1227–1229PubMedCrossRef
27.
go back to reference Young HE, Steele TA, Bray RA, Hudson J, Floyd JA, Hawkins K, Thomas K, Austin T, Edwards C, Cuzzourt J, Duenzi M, Lucas PA, Black AC Jr (2001) Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat Rec 264:51–62PubMedCrossRef Young HE, Steele TA, Bray RA, Hudson J, Floyd JA, Hawkins K, Thomas K, Austin T, Edwards C, Cuzzourt J, Duenzi M, Lucas PA, Black AC Jr (2001) Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat Rec 264:51–62PubMedCrossRef
Metadata
Title
Cd34-positive developing vessels and other structures in human fetuses: an immunohistochemical study
Authors
Shin-ichi Abe
Masashi Suzuki
Kwang Ho Cho
Gen Murakami
Baik Hwan Cho
Yoshinobu Ide
Publication date
01-12-2011
Publisher
Springer-Verlag
Published in
Surgical and Radiologic Anatomy / Issue 10/2011
Print ISSN: 0930-1038
Electronic ISSN: 1279-8517
DOI
https://doi.org/10.1007/s00276-011-0854-2

Other articles of this Issue 10/2011

Surgical and Radiologic Anatomy 10/2011 Go to the issue