Abstract
The pericytes of the testis are part of the omnipresent population of pericytes in the vertebrate body and are the only true pluripotent adult stem cells able to produce structures typical for the tree primitive germ layers: ectoderm, mesoderm, and endoderm. They originate very early in the embryogenesis from the pluripotent epiblast. The pericytes become disseminated through the whole vertebrate organism by the growing and differentiating blood vessels where they remain in specialized periendothelial vascular niches as resting pluripotent adult stem cells for tissue generation, maintenance, repair, and regeneration. The pericytes are also the ancestors of the perivascular multipotent stromal cells (MSCs). The variable appearance of the pericytes and their progeny reflects the plasticity under the influence of their own epigenetic and the local environmental factors of the host organ. In the testis the pericytes are the ancestors of the neuroendocrine Leydig cells. After activation the pericytes start to proliferate, migrate, and build transit-amplifying cells that transdifferentiate into multipotent stromal cells. These represent progenitors for a number of different cell types in an organ. Finally, it becomes evident that the pericytes are a brilliant achievement of the biological nature aiming to supply every organ with an omnipresent population of pluripotent adult stem cells. Their fascinating features are prerequisites for future therapy concepts supporting cell systems of organs.
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Abedin M, Tintut Y, Demer LL (2004) Mesenchymal stem cells and the artery wall. Circ Res 95:671–676
Alvarez-Buylla A, Seri B, Doetsch F (2002) Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 57:751–758
Angelova P, Davidoff MS (1989) Immunocytochemical demonstration of substance P in Hamster Leydig cells during ontogenesis. Z Mikrosk Anat Forsch 103:560–566
Angelova P, Davidoff MS, Baleva K, Staykova M (1991) Substance P and neuron-specific enolase-like immunoreactivity of rodent Leydig cells in tissue section and cell culture. Acta Histochem 91:131–139
Anjos-Afonso F, Bonnet D (2007) Nonhematopoietic/endothelial SSEA-1+ cells define the most primitive progenitors in the adult murine bone marrow mesenchymal compartment. Blood 109:1298–1306
Ariyaratne HB, Mendis-Handagama SMLC, Hales DB, Mason JI (2000) Studies on the onset of Leydig precursor cell differentiation in the prepubertal rat testis. Biol Reprod 63:165–171
Armulik A, Genové G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21:193–215
Attwell D, Mishra A, Hall CN, O’Farrell FM, Dalkara T (2016) What is a pericyte? J Cerebr Blood Flow Metab 36:451–455
Balabanov R, Washington R, Wagnerova J, Dore-Duffy P (1996) CNS microvascular pericytes express macrophage-like function, cell surface integrin αM, and macrophage marker ED-2. Microvasc Res 52:127–142
Barón M, Gallego A (1972) The relation of the microglia with the pericytes in the cat cerebral cortex. Z Zellforsch Mihosk Anat 128:42–57
Basciani S, Mariani S, Arizzi M, Ulisse S, Rucci N, Jannini EA, Rocca CD, Manicone A, Carani C, Spera G, Gnessi L (2002) Expression of platelet-derived growth factor-A (PDGF-A), PDGF-B, and PDGF receptor- a and -s during human testicular development and disease. J Clin Endocrinol Metab 87:2310–2319
Benninghoff A (1926) Über die Formenreihe der glatten Muskulatur und die Bedeutung der Rouget‘schen Zellen an den Kapillaren. Z Zellf Mikr Anat 4:126–170
Bensley RR, Vimtrup BJ (1928) On the nature of the Rouget cells of capillaries. Anat Rec 39:37–55
Benton L, Shan L-X, Hardy MP (1995) Differentiation of adult Leydig cells. J Steroid Biochem Mol Biol 53:61–68
Barembaum M, Bronner-Fraser M (2005) Early steps in neural crest specification. Seminars in Cell & Developmental Biology; 16(6): 642-646
Bergers G (2008) Pericytes, the mural cells of the microvascular system. In: Figg WD, Folkman J (eds) Angiogenesis. An integrative approach from science to medicine, Chapter 4. Springer, New York, pp 45–53
Bergers G, Song S (2005) The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 7:452–464
Bhagavati S (2008) Stem cell based therapy for skeletal muscle diseases. Curr Stem Cell Res Ther 3(3):219–228
Bhushan S, Meinhardt A (2017) The macrophages in testis function. J Repr Immun 119:107–112
Bianco P, Robey PG, Simmons PJ (2008) Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cells 2:313–319
Birbrair A, Delbono O (2015) Pericytes are essential for skeletal muscle formation. Stem Cell Rev Rep 11:547–548
Birbrair A, Zhank T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, Delbono O (2013a) Role of pericytes in skeletal muscle regeneration and fat accumulatioin. Stem Cells Dev 22:2298–22314
Birbrair A, Zhang T, Wang Z-M, Messi ML, Enikolopov GN, Mintz A, Delbono O (2013b) Skeletal muscle neural progenitor cells exhibit properties of NG2-glia. Exp Cell Res 319:45–63
Birbrair A, Zhang T, Files DC, Mannava S, Smith T, Wang Z-M, Messi ML, Mintz A, Delbono O (2014) Type-1 pericytes accumulate after tissue injury and produce collagen in an organ-dependent manner. Stem Cell Res Ther 5:122
Bischofberger J, Schmidt-Hieber C (2006) Adulte Neurogenese im Hippocampus. e-Neuroforum 3:212–221
Bjornson CRR, Rietze RL, Reynolds BA, Magli MC, Vescovi A (1999) Turning brain into blood: adult neural stem cells adopt a hematopoietic fate in vivo. Science 283:534–537
Bouacida A, Rosset P, Trichet V, Guilloton F, Espagnolle N, Cordonier T, Heymann D, Layrolle P, Sensébé L, Deschaseaux F (2012) Pericyte-like progenitors show high immaturity and engraftment potential as compared with mesenchymal stem cells. PLoS One 7(11):e486548
Brazelton TR, Rossi FMV, Keshet GI, Blau HM (2000) From marrow to brain: expression of neuronal phenotypes in adult mice. Science 290:1775–1779
Breau MA, Pietri T, Stemmler MP, Thiery P, Weston JA (2008) A nonneural epithelial domain of embryonic cranial neural folds gives rise to ectomesenchyme. Proc Natl Acad Sci U S A 105:7750–7755
Brennan J, Capel B (2004) One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nat Rev Gen 5(7):509–521
Brennan J, Tilmann C, Capel B (2003) Pdgfr-α mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 17:800–810
Bronner ME, Simões-Costa M (2016) The neural crest migrating into the 21st century. Curr Top Dev Biol 116:115–134
Brons IGM, Smithers LE, Trotter MWB, Rugg-Gunn P, Sun B, Lopes SMCS, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, Vallier L (2007) Derivation of pluripotent epblast stem cells from mammalian embryos. Nature 448:191–196
Buehr M, Smith A (2003) Genesis of embryonic stem cells. Philos Trans R Soc Lond B Biol Sci 358:1397–1402
Calloni GW, Glavieux-Pardanaud C, Le Douarin NM, Dupin E (2007) Sonic hedgehog promotes the development of multipotent neural crest progenitors endowed with both mesenchymal and neural potentials. Proc Natl Acad Sci U S A 104:19879–19884
Cano E, Gebala V, Gerhardt H (2017) Pericytes or mesenchymal stem cells: is that the question? Cell Stem Cell 20(3):296–297
Caplan AI (2008) All MSCs are pericytes? Cell Stem Cell 3:229–230
Cervós-Navarro J (1963) Electronenmicroscopische Befunden an den Capillaren der Hirnrinde. Arch Psych Ztschr ges Neurologie 204:484–504
Chan-Ling T (1997) Glial, vascular, and neuronal cytogenesis in whole-mounted cat retina. Microsc Res Tech 36:1–16
Chen H, Stanley E, Jin S, Zirkin BR (2010) Stem Leydig cells: From fetal to aged animals. Birth Defects Res C Embryo Today 90:272–283
Chen WCW, Baily JE, Corselli M, Diaz ME, Sun B, Xiang G, Gray GA, Huard J, Péault B (2015) Human myocardial pericytes: multipotent mesodermal precursors exhibiting cardiac specificity. Stem Cells 33:557–573
Chen H, Wang Y, Ge R, Zirkin BR (2017) Leydig stem cells: identification, proliferation and differentiation. Mol Cell Endocrinol 445:65–71
Chikhovskaya JV, Jonker MJ, Meissner A, Breit TM, Repping S, van Pelt AMM (2012) Human testis-derived embryonic stem cell-like cells are not pluripotent, but possess potential of mesenchymal progenitors. Hum Reprod 27(1):210–221
Chikhovskaya JV, van Daalen SKM, Kover CM, Repping S, van Pelt AMM (2014) Mesenchymal origin of multipotent human testis-derived stem cells in human testicular cell cultures. Mol Human Reprod 20:155–167
Chiwakata C, Brackmann B, Hunt N, Davidoff M, Schulze W, Ivell R (1991) Tachykinin (Substance P) gene expression in Leydig cells of the human and mouse testis. Endocrinology 128:2441–2448
Clark ER, Clark EL (1925a) The development of adventitial (Rouget) cells on the blood capillaries of amphibian larvae. Amer J Anat 35:239–264
Clark ER, Clark EL (1925b) The relation of Rouget cells to capillary contractility. Amer J Anat 35: 265-282
Collas P (2010) Programming differentiation potential in mesenchymal stem cells. Epigenetics 5(6):476–482
Collett GDM, Canfield AE (2005) Angiogenesis and pericytes in the initiation of ectopic calcification. Circ Res 96:930–938
Combes AN, Wilhelm D, Davidson T, Dejana E, Harley V, Sinclair A, Koopman P (2009) Endothelial cell migration directs testis cord formation. Dev Biol 326:112–120
Crane JF, Trainor PA (2006) Neural Crest stem and progenitor cells. Ann Rev Cell Dev Biol 22 (1):267-286
Crisan M, Deasy B, Gavina M, Zheng B, Huard J, Lazzari L, Péault B (2008a) Purification and long-term culture of multipotent progenitor cells affiliated with the walls of human blood vessels: myoendothelial cells and pericytes. Methods Cell Biol 86:295–309
Crisan M, Yap S, Casteilla L, Chen C-W, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng P-N, Trass J, Schugar R, Deasy BM, Badylak S, Bühring H-J, Giacobino J-P, Lazzari L, Huard J, Péault B (2008b) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313
da Silva Meirelles L, Caplan AI, Nardi NB (2013) Pericytes as the source of mesenchymal stem cells. In: Goldenberg RC d S, de Carvalho ACC (eds) Resident stem cells and regenerative therapy. Elsevier, Amsterdam, pp 233–250. https://doi.org/10.1016/B978-0-12-416012-5.00012-8
Dar A, Domev H, Ben-Yosef O, Tzukerman M, Zeevi-Levin N, Novak A, Germanguz I, Amit M, Itskovitz-Eldor J (2012) Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation 125:87–99
Davidoff MS (2017) The Leydig cells of the testis originate from the microvascular pericytes. Biomed Rev 28:5–25
Davidoff MS, Schulze W, Middendorff R, Holstein A-F (1993) The Leydig cell of the human testis—a new member of the diffuse neuroendocrine system. Cell Tiss Res 271:429–439
Davidoff MS, Middendorff R, Holstein AF (1996) Dual nature of Leydig cells of the human testis. Biomed Rev 6:11–41
Davidoff MS, Middendorff R, Koeva Y, Pusch W, Jezek D, Muller D (2001) Glial cell line-derived neurotrophic factor (GDNF) and its receptors GFR a −1 and GFR a −2 in the human testis. Ital J Anat Embryol 106(Suppl 2):p173–p180
Davidoff MS, Middendorff R, Enikolopov G, Rietmacher D, Holstein AF, Müller D (2004) Progenitor cells of the testosterone-producing Leydig cells revealed. J Cell Biol 167:935–944
Davidoff MS, Middendorff R, Müller D, Holstein AF (2009) The Neuroendocrine Leydig cells and their stem cell progenitors, the pericytes. In: Sutovsky P, Clascá F, Kmiec Z, Korf H-W, Singh B, Timmermans J-P, Schmeisser MJ (eds) Advances in anatomy, embryology and cell biology, vol 205. Springer, New York, pp 1–154
de Souza LEB, Malta TM, Kashima Hadat S, Covas DT (2016) Mesenchymal stem cells and pericytes: to what extent are they related? Stem Cells Dev 25(24):1843–1852
DeFalco T, Bhattacharya I, Williams AV, Sams DM, Capel B (2014) Yolk-sac-derived macrophages regulate fetal testis vascularization and morphogenesis. Proc Natl Acad Sci U S A 111:E2384–E2393
DeFalco T, Potter SJ, Williams AV, Waller B, Kan MJ, Capel B (2015) Macrophages contribute to the spermatogonial niche in the adult testis. Cell Rep 12:1107–1119
Dellavalle A, Sampoalesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R, Li S, Belicchi M, Peretti G, Chamberlain IS, Wright WE, Torrente Y, Ferrari S, Bianco P, Cossu G (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9:255–267
Dellavalle A, Maroli G, Covarello D, Azzoni E, Innocenti A, Perani L, Antonioni S, Sambasivan R, Brunelli S, Tajbakhsh S, Cossu G (2011) Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2:499. https://doi.org/10.1038/ncomms1508
De-Miguel MP, Arnalich-Montiel F, Lopez-Iglesias P, Blasquez-Martinez A, Nistal M (2009) Epiblast-derived stem cells in embryonic and adult tissues. Int J Dev Biol 53:1529–1540
De-Miguel MP, Fuentis-Julian S, Alcaina Y (2010) Pluripotent stem cells: origin, maintenance and induction. Stem Cell Rev Rep 6:633–649
Denham M, Hasegawa K, Menheniott T, Rollo B, Zhang D, Hough S, Alshawa A, Febbraro F, Ighanian S, Leung J, Elliott DA, Newgreen DF, Pera MF, Dottori M (2015) Multipotent caudal neural progenitors derived from humans pluripotent stem cells that give rise to lineages of the central and peripheral nervous system. Stem Cells 33(6):1759–1770
Diaz-Flores L Jr, Madrid JF, Guitérrez R (2006) Adult stem and transit-amplifying cell location. Histol Histopathol 21:995–1027
Diaz-Flores L, Gutiérrez R, Madrid JF, Varela H, Valladares F, Acosta E, Martin-Vasallo P, Diaz-Flores L Jr (2009) Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 24:909–969
Diaz-Flores L, Gutiérrez R, Garcia MP, Diaz-Flores L Jr, Valladares F, Madrid JF (2012) Ultrastructure of myopericytoma: a continuum of transitional phenotypes of myopericytes. Ultrastr Pathol 36:189–194
Doetsch F (2003) The glial identity of neural stem cells. Nat Neurosci 6:1127–1134
Dogiel AS (1899) Über den Bau der Ganglien in den Geflechten des Darms und der Gallenblase des Menschen und der Säugetiere. Arch Anat Physiol Anat Abt A 3–4:100–158
Donoghue PCJ, Graham A, Kelsh RN (2008) The origin and evolution of the neural crest. BioEssays 30:530–541
Dore-Duffy P (2008) Pericytes: pluripotent cells of the blood brain barrier. Curr Pharm Des 14(16):1581–1593
Dore-Duffy P, Cleary K (2011) Morphology and properties of pericytes. Meth Mol Biol 686(Part 1):49–68
Eberth CJ (1871) Von den Blutgefässen. Capitel VIII. In: Stricker S (ed) Handbuch der Lehre von den Geweben des Menschen und der Tiere, Bd 1. Verlag von Wilhelm Engelmann, Leipzig, pp 191–213
Ergün S, Stingl J, Holstein AF (1994) Microvasculature of the human testis in correlation to Leydig cells and seminiferous tubules. Andrologia 26(5):255–262
Ergün S, Davidoff M, Holstein AF (1996) Capillaries in the lamina propria of human seminiferous tubules are partly fenestrated. Cell Tissue Res 286(1):93–102
Ergün S, Harneit S, Paust HJ, Mukhopadhyay AK, Holstein AF (1999) Endothelin and endothelin receptors A and B in the human testis. Anat Embryol 199:207–214
Etchevers HC, Vincent C, Le Douarin NM, Couly GF (2001) The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 128:1059–1068
Fawcett DW, Neaves WB, Flores MN (1973) Comparative observations on intertubular lymphatics and the organization of the interstitial tissue of the mammalian testis. Biol Reprod 9:500–532
Fecteau KA, Markonjich L, Mason JI, Mendis-Handagama SMLC (2006) Detection of platelet-derived growth factor-α (PDGF-A) protein in cells of Leydig lineage in the postnatal rat testis. Histol Histopathol 21:1295–1302
Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang L-P, Yamaguchi M, Kettenmann H, Kempermann G (2003) Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 23:373–382
Fisher M, (2009) Pericyte signaling in the neurovascular unit. Stroke 40 (3, Suppl 1):S13-S15
Flamme I, Frölich T, Risau W (1997) Molecular mechanisms of vasculogenesis and embryonic angiogenesis. J Cell Physiol 173:206–210
Florey HW, Carleton HM (1926) Rouget cells and their function. Proc R Soc Lond B 100:23–31
Friedrich R, Holstein AF, Middendorff R, Davidoff MS (2012) Vascular wall cells contribute to tumorigenesis in cutaneous neurofibromas of patients with Neurofibromatosis type 1. A comparative histological, ultrastructural and immunohistochemical study. Anticancer Res 32:2139–2158
Ge R-S, Dong Q, Sottas CM, Papadopoulos V, Zirkin BR, Hardy MP (2006) In search of rat stem Leydig cells: identification, isolation, and lineage-specific development. Proc Natl Acad Sci U S A 103:2719–2724
Gilbert SF (2000) The Neural Crest. Developmental Biology, 6th edn. Sinauer Associates, Sunderland, MA. Available from: https://www.ncbi.nlm.nih.gov/books/NBK10065/
Griswold SL, Behringer RR (2009) Fetal Leydig cell origin and development. Sexual Development 3 (1):1–15
Gnessi L, Emidi A, Jannini EA, Carosa E, Maroder M, Arizzi M, Ulisse S, Spera G (1995) Testicular development involves the spatiotemporal control of PDGFs and PDGF receptors gene expression and action. J Cell Biol 131:1105–1121
Gnessi L, Basciani S, Mariani S, Arizzi M, Spera G, Wang C, Bondjers C, Karlsson L, Betsholtz C (2000) Leydig cell loss and spermatogenic arrest in platelet-derived growth factor (PDGF)-A-deficient mice. J Cell Biol 149(5):1019–1025
Gökçinar-Yagei B, Uçkan-Çetinkaya D, Çelebi-Saltik B (2015) Pericytes: Properties, functions and applications in tissue engineering. Stem Cell Rev Rep 11:549–559
Goluža T, Boscanin A, Cvetko J, Kozina V, Kosoviċ M, Bernat MM, Kasum M, Kaštelan Ž, Ježek D (2014) Macrophages and Leydig cells in testicular biopsies of azoospermic men. Biomed Res Int 2014:828697, 14 pages
Gondos B (1980) Development and differentiation of the testis and male reproductive tract. In: Steinberger A, Steinberger E (eds) Testicular development structure and function. Raven, New York, pp 3–20
Gonzalez R, Griparic L, Vargas V, Burgee K, Santacruz P, Anderson R, Schiewe M, Silva F, Patel A (2009) A putative mesenchymal stem cells population isolated from adult human testes. Biochem Biophys Res Commun 385:570–575
Gonzalez-Perez O (2012) Neural stem cells in the adult human brain. Biol Biomed Rep 2(1):59–69
Guimarães-Camboa N, Cattaneo P, Sun Y, Moore-Morris T, Gu Y, Dalton ND, Rockenstein E, Masliah E, Peterson KL, Stallcup WB, Chen J, Evans SM (2017) Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell 20(3):345–359
Günther H (1917) Die mechanische Erregbarkeit der Hautmuskeln und Hautgefäße. In: Kraus F et al (eds) Ergebnisse der Inneren Medizin und Kinderheilkunde, vol 15. Julius Springer, Berlin, pp 620–714
Haider SG, Servos K, Tran N (2007) Structural and histological analysis of Leydig cell steroidogenic function. In: Payne AH, Hardy MP (eds) Contemporary endocrinology: the Leydig cell in health and disease. Humana Press, Totowa, NJ, pp 33–45
Hall BK (1998) Germ layers and the germ-layer theory revisited: Primary and secondary germ layers, neural crest as a fourth germ layer, homology, demise of the germ-layer theory. Evol Biol 30:121–186
Hall BK (2000) The neural crest as a fourth germ layer and vertebrates as quadroblastic not triploblastic. Evol Dev 2:3–5
Hall AP (2006) Review of the pericyte during angiogenesis and its role in cancer and diabetic retinopathy. Toxicol Pathol 34:763–775
Hara Y, Nomura T, Yoshizaki K, Frisén J, Osumi N (2010) Impaired hippocampal neurogenesis and vascular formation in ephrin-A5-deficient mice. Stem Cells 28:974–983
Hermann M, Bara JJ, Sprecher CM, Menzel U, Jalowiec JM, Osinga R, Scherberich A, Alini M, Verrier S (2016) Pericyte plasticity—comparative investigation of the angiogenic and multilineage potential of pericytes from different human tissues. Eur Cells Mater 31:236–249
Hill JP, Watson KM (1958) The early development of the brain in marsupials preliminary communication. J Anat 92(Pt4):493–497
Hill WD, Hess DC, Martin-Studdard A, Carotheres JJ, Zheng J, Hale D, Maeda M, Fagan SC, Carroll JE, Conway SJ (2004) SDF-1 (CXCL12) is upregulated in the ischemic penumbra following stroke: association with bone marrow cell homing to injury. J Neuropathol Exp Neurol 63:84–96
Hirschi KK, D’Amore PA (1996) Pericytes in the microvasculature. Cardiovasc Res 32:687–698
Holstein AF (1999) Spermatogenese beim Menschen: Grundlagenforschung und Klinik. Ann Anat 181:427–436
Holstein AF, Davidoff MS (1997) Organization of the intertubular tissue of the human testis. In: Motta PM (ed) Recent advances of cells, tissues and organs. Antonio Delfino Editore, Rome, pp 569–577
Holstein AF, Maekawa M, Nagano T, Davidoff MS (1996) Myofibroblasts in the lamina propria of human seminiferous tubules are dynamic structures of heterogeneous phenotype. Arch Histol Cytol 59:109–125
Holstein AF, Schulze W, Davidoff M (2003) Understanding spermatogenesis is a prerequisite for treatment. Reprod Biol Endocrinol 1:107
Hosaka K, Yang Y, Sekia T, Fischera C, Dubeya O, Fredlundc E, Hartman J, Religa P, Morikawa H, Ishii Y, Sasahara M, Larsson O, Cossu G, Cao R, Lim S, Cao Y (2016) Pericyte–fibroblast transition promotes tumor growth and metastasis. Proc Natl Acad Sci U S A 113(38):E5618–E5627
Huhtaniemi I, Pelliniemi LJ (1992) Fetal Leydig cells: cellular origin, morphology, life span, and special functional features. Proc Soc Exp Biol Med 201:125–140
Itoh Y, Toriumi H, Yamada S, Hoshino H, Suzuki N (2011) Astrocytes and pericytes cooperatively maintain a capillary-like structure composed of endothelial cells on gel matrix. Brain Res 1406:74–83
Jiang Y, Hernderson D, Blackstad M, Chen A, Miller RF, Verfaillie CM (2003) Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc Natl Acad Sci U S A 100:11854–11860
Joseph NM (2004) Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneurial fibroblasts in addition to Schwann cells. Development 131 (22):5599-5612
Kahn CR (2008) Can we nip obesity in its vascular bud? Science 322:542–543
Kastschenko N (1888) Zur Entwicklungsgeschichte des Salachierembryos. Anatomischer Anzeiger III (1–32) 16:445–467
Kaufman M (1992) The atlas of mouse development. Academic, London, p 512
Kennedy E, Mooney CJ, Hakimjavadi R, Fitzpatrick E, Guha S, Collins LE, Loscher CE, Morrow D, Redmond EM, Cahill PA (2014) Adult vascular smooth muscle cells in culture express neural stem cell markers typical of resident multipotent vascular stem cells. Cell Tissue Res 358:203–216
Kerr JB, Sharpe RM (1985) Stimulatory effect of follicle-stimulating hormone on rat Leydig cells. A morphometric and ultrastructural study. Cell Tissue Res 239:405–415
Kerr JB, Donachie K, Rommerts FFG (1985) Selective destruction and regeneration of rat Leydig cells in vivo. Cell Tiss Res 242:145–156
Kerr JB, Bartlett JMS, Donachie K (1986) Acute response of testicular interstitial tissue in rats to the cytotoxic drug ethane dimethanesulphonate. An ultrastructural and hormonal study. Cell Tissue Res 243:405–414
Kerr JB, Knell CM, Abbott M, Donachie K (1987a) Ultrastructural analysis of the effect of ethane dimethanesulphonate on the testis of the rat, guinea pig, hamster and mouse. Cell Tissue Res 249:451–457
Kerr JB, Bartlett JMS, Donachie K, Sharpe RM (1987b) Origin of regenerating Leydig cells in the testis of the adult rat. An ultrastructural, morphometric and hormonal assay study. Cell Tissue Res 249:367–377
Kilcoyne KR, Smith LB, Atanassova N, Macpherson S, McKinell C, van den Driesche S, Jobling MS, Ghambers TJG, De Gendt K, Verhoeven G, O’Hara L, Platts S, de Franca LR, Lara NLM, Anderson RA, Sharpe RM (2014) Fetal programming of adult Leydig cell function by androgenic effects on stem/progenitor cells. Proc Natl Acad Sci U S A 111:E1924–E1932
Klein D, Weißhardt P, Kleff V, Jastrow H, Jakob HG, Ergün S (2011) Vascular wall-resident CD44+ multipotent stem cells give rise to pericytes and smooth muscle cells and contribute to new vessel maturation. PLoS One 6:e20540
Klein D, Meissner N, Kleff V, Jastrow H, Yamaguchi M, Ergün S, Jendrossek V (2014) Nestin(+) tissue-resident multipotent stem cells contribute to tumor progression by differentiating into pericytes and smooth muscle cells resulting in blood vessel remodeling. Front Oncol 4:Article 169
Kojima Y, Kaufman-Francis K, Studdert JB, Steiner KA, Power MD, Loebel DAF, Jones V, Hor A, de Alencastro G, Logan GJ, Teber ET, Tam OH, Stutz MD, Alexander IE, Pickett HA, Tam PPL, (2014) The transcriptional and functional properties of mouse epiblast stem cells resemble the anterior primitive streak. Cell Stem Cell 14 (1):107–120
Krogh A (1919) The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue. J Physiol 52:409–415
Krogh A (1922) The anatomy and physiology of the capillaries. New Haven Yale University Press, London, pp 1–304
Krogh A (1929) Anatomie und Physiologie der Capillaren. p.362, Springer, Berlin-Heidelberg.
Krueger M, Bechmann I (2010) CNS pericytes: concepts, misconceptions, and a way out. Glia 58:1–10
Kucia M, Reca R, Jala VR, Dawn B, Ratajczak J, Ratajczak MZ (2005) Bone marrow as a home of heterogeneous populations of nonhematopoietic stem cells. Leukemia 19:1118–1127
Kucia M, Machalinski B, Ratajczak MZ (2006) The developmental deposition of epiblast/germ cell-line derived cells in various organs as a hypothetical explanation of stem cell plasticity? Acta Neurobiol Exp 66:331–341
Kurtz A (2016) Commentary for “human kidney pericytes produce renin”. Kidney Int 90:1153–1154
Landreh L, Stukenborg J-B, Söder O, Svechnikov K (2013) Phenotype and steroidogenic potential of PDGFα-positive rat neonatal peritubular cells. Mol Cell Endocrinol 372:96–104
Landreh L, Spinner K, Schubert K, Häkkinen MR, Auriola S, Poutanern M, Söder O, Svechnikov K, Mayerhofer A (2014) Human testicular peritubular cells host putative stem Leydig cells with steroidogenic capacity. J Clin Endocrinol Metab 99(7):E1227–E1235
Le Douarin NM, Dupin E (2003) Multipotentiality of the neural crest. Current Opinion in Genetics & Development 13 (5):529–536
Le Douarin NM, Callani GW, Dupin E (2008) The stem cells of the neural crest. Cell Cycle 7:1013–1019
Lee RTH, Knapik EW, Thiery JP, Carney TJ (2013a) An exclusively mesodermal origin of fin mesenchyme demonstrates that zebrafish trunk neural crest does not generate ectomesenchyme. Development 140:2923–2932
Lee RTH, Negai H, Nakaya Y, Sheng G, Trainor PA, Weston JA (2013b) Cell delamination in the mesencephalic neural fold and its implication for the origin of ectomesenchyme. Development 140:4890–4902
Leeson TS, Cookson FB (1974) The mammalian testicular capsule and its muscle elements. J Morph 144:237–254
Lindner U, Kramer J, Rohwedel J, Schlenke P (2010) Mesenchymal stem or stromal cells: toward a better understanding of their biology? Transfus Med Hemother 37:75–83
Ling E-A, Wong W-C (1993) The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 7:9–18
Louissaint A Jr, Rao S, Leventhal C, Goldman SA (2002) Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34(6):945–960
Maekawa M, Kamimura K, Nagano T (1996) Peritubular myoid cells in the testis: their structure and function. Arch Histol Cytol 59:1–13
Makala H, Pothana L, Sonam S, Malla A, Goel S (2015) Regeneration of Leydig cells in ectopically autografted adult mouse testis. Reproduction 149:259–268
Mariani S, Basciani S, Arizzi M, Spera G, Gnessi L (2002) PDGF and the testis. Trends Endocrinol Metab 13(1):11–17
Mayer S (1902) Die Muskularisierung der capillaren Blutgefäße. Nachweis des anatomischen Substrats ihrer Kontraktilität. Anat Anz, Jena 21:442–455
McLaren A (2003) Primordial germ cells in the mouse. Dev Biol 262:1–15
Michels NA (1936) The structure of capillaries and the un-myogenic character of Rouget cells (Pericytes) in the omentum of rabbits and the web of living frogs. Anat Rec 65:99–125
Middendorff R , Davidoff MS , Holstein AF (1993) Neuroendocrine marker substances in human Leydig cells – changes by disturbances of testicular function. Andrologia; 25:257–262
Middendorff R, Müller D, Mewe M, Mukhopadhyay AK, Holstein A-F, Davidoff MS (2002) The tunica albuginea of the human testis is characterized by complex contraction and relaxation activities regulated by cyclic GMP. J Clin Endocrinol Metab 87:3486–3499
Millner R, Hung S, Erokwu B, Dore-Duffy P, LaManna JC, del Zoppo GJ (2008) Increased expression of fibronectin and the α5ß1integrin angiogenic cerebral blood vessels of mice subject to hypobaric hypoxia. Mol Cell Neurosci 38:43–52
Mizrak SC, Chikhovskaya JV, Sadri-Ardekani H, van Daalen S, Korver CM, Hovingh SE, Roepers-Gajadien HL, Raya A, Fluiter K, de Reijke TM, de la Rosette JJMCH, Knegt AC, Belmonte JC, van der Veen F, de Rooij DG, Repping S, van Pelt AMM (2010) Embryonic stem cell-like cells derived from adult human testis. Hum Reprod 25:158–167
Molenaar R, de Rooij DG, Rommerts FFG, Reuvers PJ, van der Molen HJ (1985) Specific destruction of Leydig cells in mature rats after in vivo administration of Ethane dimethyl sulfonate. Biol Reprod 33:1213–1222
Montiel-Eulefi E, Sánchez R, Rojas M, Bustos-Obregon E (2009) Epiblast embryo stem cells give origin to adult pluripotent cell populations: primordial germ cell, pericytic and haematopoietic stem cells. A review. Int J Morphol 27:1325–1333
Mori S, Leblond CP (1969) Identification of microglia in light and electron microscopy. J Comp Neurol 135:57–79
Morshead CM (2004) Adult neural stem cells: attempting to solve the identity crisis. Dev Neurosci 26:93–199
Müller I (1957) Kanälchen—und Capillararchitektonik des Rattenhodens. Z Zellforsch 45:522–537
Murakami T, Uno Y, Ohtsuka A, Taguchi T (1989) The blood vascular architecture of the rat testis: a scanning electron microscopic study of corrosion casts followed by light microscopy of tissue sections. Arch Histol Cytol 52:151–172
Murray IR, West CC, Hardy WR, James AW, Park TS, Nguyen A, Tawonsawatruk T, Lazzari L, Soo C, Péault B (2014) Natural history of mesenchymal stem cells, from vessel walls to culture vessels. Cell Mol Life Sci 71(8):1353–1374
Nakagawa T, Nabeshima Y, Yoshida S (2007) Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 12(2):195–206
Newgreen DF, Kerr RS, Minichiello J, Warren N (1997) Changes in cell adhesion and extracellular matrix molecules in spontaneous spinal neural tube defects in avian embryos. Teratology 55:195–207
Nichols DH (1981) Neural crest formation in the head of the mouse embryo as observed using a new histological technique. J Embryol Exp Morph 64:105–120
Nichols DH (1986) Formation and distribution of neural crest mesenchyme to the first pharyngeal arch region of the mouse embryo. Am J Anat 176:221–231
Nichols J, Smith A (2012) Pluripotency in the embryo and in culture. Cold Spring Harbor Perspectives in Biology 4 (8):a008128-a008128
Nikolova G, Strilic B, Lammert E (2007) The vascular niche and its basement membrane. Trends Cell Biol 17:19–25
Ochs K, Sahm F, Opitz CA, Lanz TV, Oezen I, Couraud P-O, von Deimling A, Wick W, Platten M (2013) Immature mesenchymal stem cell-like pericytes as mediators of immunosuppression in human malignant glioma. J Neuroimmunol 265:106–116
Ortega HH, Lorente JA, Salvetti NR (2004a) Immunohistochemical study of intermediate filaments and neuroendocrine marker expression in Leydig cells of laboratory rodents. Anat Histol Embryol 33(5):309–315
Orth J, Weisz J (1980) Development of Δ5-3ß-hydroxysteroid dehydrogenase and glucose-6- phosphatase activity in Leydig cells of the fetal rat testis: a quantitative cytochemical study. Biol Reprod 22:1201–1209
Özen I, Boix J, Paul G (2012) Perivascular mesenchymal stem cells in the adult human brain: a future target for neuroregeneration? Clin Transl Med 1(1):30
Pacini S, Petrini I (2014) Are MSCs angiogenic cells? New insights on human nestin-positive bone-marrow-derived multipotent cells. Front Cell Dev Biol 2:Article 20. https://doi.org/10.3389/fcell.2014.00020
Palm T, Nielsen SL, Lassen NA (1983) Vascular recruitment in forearm muscles during exercise. Clin Physiol 3:445–451
Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479–494
Paniagua R, Rodriguez MC, Nistal M, Fraile B, Regadera J, Amat P (1988) Changes in surface area and number of Leydig cells in relation to the 6 stages of the cycle of the human seminiferous epithelium. Anat Embryol 178(5):423–427
Péault B, Rudnicki M, Torrente Y, Cossu G, Trmblay JP, Partridge T, Gussoni E, Kunkel LM, Huard J (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15:867–877
Ratajczak MZ, Machalinski B, Wojakowski W, Ratajczak J, Kucia M (2007) A hypothesis for embryonic origin of pluripotent Oct-4+ stem cells in adult bone marrow and other tissues. Leukemia 21:860–867
Ratajczak MZ, Zuba-Surma EK, Wysoczynski M, Ratajczak J, Kucia M (2008) Very small embryonic-like stem cells: characterization, developmental origin, and biological significance. Exp Hematol 36:742–751
Ratajczak MZ, Shin D-M, Liu R, Mierzeiewska K, Ratajczak J, Kucia M, Zuba-Surma EK (2012a) Very small embryonic/epiblast-like stem cells (VSELs) and their potential role in aging and organ rejuvenation—an update and comparison to other small stem cells isolated from adult tissues. Aging 4:235–246
Ratajczak MZ, Zuba-Surma E, Kucia M, Poniewierska A, Suszynska M, Ratajchak J (2012b) Pluripotent and multipotent stem cells in adult tissues. Adv Med Sci 57:1–17
Ribatti D, Vacca A (2008) Overview of angiogenesis during tumor growth, Chapter 14. In: Figg WD, Folkman J (eds) Angiogenesis. An integrative approach from science to medicine. Springer, New York, NY, pp 161–167
Ribatti D, Nico B, Crivellato E (2011) The role of pericytes in angiogenesis. Int J Dev Biol 55:261–268
Rolandsson S, Andersson Sjöland A, Brune JC, Li H, Kassem M, Martens F, Westergren A, Eriksson L, Hanson L, Skog I, Bjermer L, Scheding S, Westergren-Thorson G (2014) Primary mesenchymal stem cells in human transplanted lungs are CD90/CD105 perivascularly located tissue-resident cells. BMJ Open Resp Res 1:e000027. https://doi.org/10.1136/bmjresp-2014-00002
Rossant J (2001) Stem cells from the mammalian blastocyst. Stem Cells 19:477–482
Rouget CMB (1873) Memoiré sur le développment, la structure et les propriétés physiologiques des capillaires sanguins et lymphatiques. Arch Physiol 5:603–661
Rouget CMB (1879) Sur la contractilite des capillaires sanguins. Compt Rend Acad Sci Paris 88:916–918
Rowley JE, Johnson JR (2014) Pericytes in chronic lung disease. Int Arch Allergy Immunol 164:178–188
Russell LD, de França LR (1995) Building a testis. Tissue Cell 27:129–147
Sá-Pereira I, Brites D, Brito MA (2012) Neurovascular unit: a focus on pericytes. Mol Neurobiol 45:327–347
Sbanti RM, Li W-J, Nesti LJ, Wang Y, Tuan RS (2007) Adult mesenchymal stem cells: biological properties, characteristics, and application in maxillofacial surgery. J Oral Maxillofac Surg 65:1640–1647
Scadden DT (2006) The stem-cell niche as an entity of action. Nature 44:1075–1079
Schulze W, Davidoff MS, Holstein A-F (1987) Are Leydig cells of neural origin? Substance P-like immunoreactivity in human testicular tissue. Acta Endocrinol 115:373–377
Shan L-X, Hardy MP (1992) Developmental changes in levels of luteinizing hormone receptor and androgen receptor in rat Leydig cells. Endocrinology 131:1107–1114
Shan L-X, Zhu L-J, Bardin CW, Hardy MP (1995) Quantitative analysis of androgen receptor messenger ribonucleic acid in developing Leydig cells and Sertoli cells by in situ hybridization. Endocrinology 136:3856–3862
Shan L-X, Bardinb CW, Hardy MP (1997) Immunohistochemical analysis of androgen effects on androgen receptor expression in developing Leydig and Sertoli cells. Endocrinology 138:1259–1266
Sharpe RM (1994) Regulation of spermatogenesis. In: Knobil E, Neil JD (eds) The physiology of reproduction, vol 1, 2nd edn. Raven Press, New York, pp 1363–1434
Shen C-N, Burke ZD, Tosh D (2004a) Transdifferentiation, metaplasia and tissue regeneration. Organogenesis 1:36–44
Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004b) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338–1340
Shen Q, Wang W, Kokovay E, Lin G, Chang S-M, Goderie SK, Roysam B, Temple S (2008) Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche-cell interactions. Cell Stem Cell 3:289–300
Shibata H, Ikeda Y, Mukai T, K-i M, Kurihara I, Ando T, Suzuki T, Kobayashi S, Murai M, Saito I, Saruta T (2001) Expression profiles of COUP-TF, DAX-1, and SF-1 in human adrenal gland and adrenocortical tumors: possible implications in steroidogenesis. Mol Gen Metabol 74:206–216
Shyamala K, Yanduri S, Girish HC, Murgod S (2015) Neural crest: the fourth germ layer. J Oral Maxillofac Pathol 19(2):221–229
Sild M, Rithazer ES (2011) Radial glía: progenitor, pathway, and partner. Neuroscience 17(3):288–302
Sims DE (1986) The pericyte—a review. Tiss Cell 18:153–174
Skinner MK, Tung PS, Fritz IB (1985) Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components. J Cell Biol 100:1941–1947
Smith AG (2001) Embryo-derived stem cells: of mice and men. Annu Rev Cell Dev Biol 17:435–462
Soncin F, Ward CM (2011) The function of E-cadherin in stem cell pluripotency and self- renewal. Genes 2:229–259
Spence SG, Poole TJ (1994) Developing blood vessels and associated extracellular matrix as substrates for neural crest migration in Japanese quail, Coturnix coturnix japonica. Int J Dev Biol 38:85–98
Stanley EL, Johanston DS, Fan J, Papadopoulos V, Chen H, Ge RS, Zirkin BR, Jelinsky SA (2011) Stem Leydig cell differentiation: gene expression during development of the adult rat population of Leydig cells. Biol Reprod 85:1161–1166
Stanley E, Lin C-Y, Jin S, Liu J, Sottas CM, Ge R, Zirkin BR, Chen H (2012) Identification, prtoliferation, and differentiation of adult Leydig stem cells. Endocrinology 153:5002–5010
Suzuki F, Nagano T (1986) Microvasculature of the human testis and excurrent duct system. Resin-casting and scanning electron-microscopic studies. Cell Tissue Res 243:79–89
Svingen T, Koopman P (2013) Building the mammalian testis: origins, differentiation, and assembly of the component cell populations. Genes Dev 27:2409–2426
Takamoto N (2005) COUP-TFII is essential for radial and anteroposterior patterning of the stomach. Development 132 (9):2179–2189
Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD, Graff JM (2008) White fat progenitor cells reside in the adipose vasculature. Science 322:583–586
Tavazoie M, Van der Veke L, Silva-Varga V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F (2008) A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3:279–288
Teerds K (1996) Regeneration of Leydig cells after depletion by EDS: a model for postnatal Leydig cell regeneration. In: Payne AH, Hardy MP, Russel LD (eds) The Leydig cell. Cache River, Vienna, pp 203–219
Teerds K, Rijntjes E (2007) Dynamics of Leydig cell regeneration after EDS. A model for postnatal Leydig cell development. In: Payne AH, Hardy MP (eds) Contemporary endocrinology: the Leydig cell in health and disease. Humana Press, Totowa, NJ, pp 91–116
Teerds KJ, de Boer-Brouwer M, Dorrington JH, Balvers M, Ivell R (1999) Identification of markers for precursor and Leydig cell differentiation in the adult rat testis following ethane dimethyl sulphonate administration. Biol Reprod 60:1437–1445
Teerds KJ, Rijntjes E, Veldhuizen-Tsoerkan MB, Rommerts FFG, de Boer-Brouwer M (2007) The development of rat Leydig cell progenitors in vitro: how essential is luteinizing hormone? J Endocrinol 194:579–593
Thiery JP, Delouvee A, Gallin W, Cunningham B, Edelman G (1984) Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers. Dev Biol 102:61–78
Thomas WE (1999) Brain macrophages: on the role of pericytes and perivascular cells. Brain Res Rev 31:42–57
Tosh D, Slack JMW (2002) How cells change their phenotype. Nat Rev 3:187–194
Trainor PA, Melton KR, Manzanares M (2003) Origins and plasticity of neural crest cells and their roles in jaw and craniofacial evolution. Int J Dev Biol 47: 541–553
Trainor PA (2005) Spezification and pattering of neural crest cells during craniofacial development. Brain Behav Evol 66: 266–280
Traktuev DO, Merferld-Clauss S, Li J, Kolonin M, Arap W, Pasqualini R, Johnstone BH, March KL (2008) A population of multipotent CD-34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 102:77–85
Trost A, Lange S, Schroedl F, Bruckner D, Motloch KA, Bogner B, Kaser- Eichberger A, Strohmaier C, Runge C, Aigner L, Rivera FJ, Reitsamer HA (2016) Brain and retinal pericytes: origin, function and role. Front Cell Neurosci 10:20
van Dijk CGM, Nieuweboer FE, Pei JY, Xu YJ, Burgisser P, van Mulligen E, el Azzouzi H, Duncker DJ, Verhaar MC, Cheng C (2015) The complex mural cell: pericyte function in health and disease. Int J Cardiol 190:75–89
Vimtrup B (1922) Beiträge zur Anatomie der Capillaren. I. Über contractile Elemente in der Gefäßwand der Blutcapillaren. Anat Embryol 65:150–182
Wang L, Kamath A, Frye J, Iwamoto GA, Chun JL, Berry SE (2012) Aorta-derived mesoangioblasts differentiate into the oligodendrocytes by inhibition of the Rho kinase signaling pathway. Stem Cells Dev 7:1069–1189
Weerasooriya TR, Yamamoto T (1985) Three-dimensional organization of the vasculature of the rat spermatic cord and testis. Cell Tissue Res 241:317–323
Wei LC, Shi M, Chen LW, Cao R, Zhang P, Chan YS (2002) Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Brain Res Dev Brain Res 139:9–17
Welsh M, Saunders PT, Atanassova N, Sharpe R, Smith LB (2009) Androgen action via testicular peritubular myoid cells is essential for male fertility. FASEB J 23:4218–4230
Welsh M, Sharpe RM, Moffat L, Atanassova N, Saunders PTK, Kilter S, Bergh A, Smith LB (2010) Androgen action via testicular arteriole smooth muscle cells is important for Leydig cell function, vasomotion and testicular fluid dynamics. PLoS One 5(10):e13632
Welsh M, Moffat L, Belling K, de França LR, Segatelli TM, Saunders PTK, Sharpe RM, Smith LB (2011) Androgen receptor signaling in peritubular myoid cells is essential for normal differentiation and function of adult Leydig cells. Int J Androl 35:25–40
Weston JA, Thiery JP (2015) Pentimento: neural crest and the origin of mesectoderm. Dev Biol 401:37–61
Weston JA, Yoshida H, Robinson V, Nishikawa S, Fraser ST, Nishikawa S (2004) Neural crest and the origin of ectomesenchyme: neural fold heterogeneity suggests an alternative hypothesis. Dev Dyn 229:118–130
Wong SP, Rowley JE, Redpath AN, Tilman JD, Fellous TG, Johnson JR (2015) Pericytes, mesenchymal stem cells and their contributions to tissue repair. Pharmacol Ther 151:107–120. https://doi.org/10.1016/j.pharmthera.2015.03.006
Yao HH-C, Barsoum I (2007) Fetal Leydig cells. Origin, regulation, and function. In: Payne AH, Hardy MP (eds) Contemporary endocrinology: The Leydig Cell in Health and Disease. Humana Press, Totowa, pp. 47-54
Ye L, Li X, Li L, Chen H, Ge R-S (2017) Insights into the development of the adult Leydig cell lineage from stem Leydig cells. Front Physiol 8:430
Yoshida S, Sukeno M, Nabeshima Y-I (2007) A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317:1722–1726
Yoshimizu T, Obinata M, Matsui Y (2001) Stage-specific tissue and cell interactions play key roles in mouse germ cell specification. Development 128: 481–490
You LR, Lin F-J, Lee CT, DeMayo FJ, Tsai M-J, Tsai SY (2005) Suppression of notch signaling by COUP-TFII transcription factor regulates vein identity. Nature 435:98–104
Zhu X, Bergles DE, Nishiyama A (2008) NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135:145–157
Zimmerlin L, Donnenberg VS, Pfeifer ME, Meyer EM, Péault B, Rubin JP, Donnenberg AD (2010) Stromal vascular progenitors in adult human adipose tissue. Cytometry A 77A:22–30
Zimmerlin L, Donnenberg VS, Donnenberg AD (2012) Pericytes: A universal adult tissue stem cell? Cytometry A 81A: 12-14 doi:10.1002/cyto.a21168
Zimmermann KW (1923) Der feinere Bau der Blutcapillaren. Zeitschr f d ges Anat I Abt 68:29–109
Zouani OF, Lei Y, Durrieu M-C (2013) Pericytes, stem-cell-like cells, but not mesenchymal stem cells are recruited to support microvascular tube stabilization. Small 9:3070–3075
Zwaka TP, Thomson JA (2005) A germ cell origin of embryonic stem cells? Development 132:227–233
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Davidoff, M.S. (2019). The Pluripotent Microvascular Pericytes Are the Adult Stem Cells Even in the Testis. In: Birbrair, A. (eds) Pericyte Biology in Different Organs. Advances in Experimental Medicine and Biology, vol 1122. Springer, Cham. https://doi.org/10.1007/978-3-030-11093-2_13
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