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The Leydig Cells of the Testis Originate from the Microvascular Pericytes

Michail S. Davidoff

Abstract

This review offers some clarifying thoughts about the nature and origin of the fetal and adult Leydig cells, supporting the conception that the pericytes (the periendothelial cells) and the smooth muscle cells of the microvasculature, that represent the main omnipresent adult stem cell population of the mammalian organism, are the Leydig cell ancestors. Our attention is specifically dedicated to the numerous contradictions as well as ambiguities concerning the hypotheses that the mesenchymal stromal cells (MSCs), the neural crest stem cells (NCSCs) and the peritubular myoid stem cells (PMCs) represent the stem ancestors of the Leydig cells. In effect, it becomes evident that the only pluripotent stem cell-like cells in the vertebrate body, including the testis, are the pericytes. The pericytes are derivate of the embryonal epiblast and retain its pluripotency within the microvascular niches where they are disseminated during the embryo- and fetogenesis and are stored as a resting adult stem cell population for tissue generation, maintenance, repair and regeneration. The pluripotency of the epiblast and the pericytes themselves are responsible and explain the neural features of the Leydig cells. Thus, both NCSCs and PMCs are not the ancestors of the pericytes, respectively of the Leydig cells. Biomed Rev 2017; 28: 1-21.

Keywords: Leydig cells, origin, microvascular pericytes, smooth muscle cells, Leydig stem cells


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References

Schulze W, Davidoff MS, Holstein A-F. Are Leydig cells of neural origin? Substance P-like immunoreactivity in human testicular tissue. Acta Endocrinologica (Copenh) 1987; 115: 373-377. DOI: 10.1530/ acta.0.1150373

Davidoff MS, Schulze W, Middendorff R, Holstein A-F. The Leydig cell of the human testis – a new member of the diffuse neuroendocrine system. Cell Tiss Res 1993; 271: 429-439.

Davidoff MS, Middendorff R, Holstein AF. Dual nature of Leydig cells of the human testis. Biomed Rev 1996; 6: 11-41.

Ortega HH, Lorente JA, Salvetti NR. Immunohistochemical study of intermediate filaments and neuroendocrine marker expression in Leydig cells of laboratory rodents. Anat Histol Embryol 2004; 33: 309-315 DOI: 10.1111/j.1439-0264.2004.00559.x

Ortega HH, Lorente JA, Mira GA, Baravalle C, Salvetti NR. Constant light exposure causes dissociation in gonadotrophin secretion and inhibits partially neuroendocrine differentiation of Leydig cells in adult rats. Reprod Domest Anim 2004; 39: 417-443. DOI: 10.1111/j.1439-0531.2004.00541.x

Ortega HH, Salvetti NR, Baravalle C, Lorente JA, Mira GA. Oestradiol induced inhibition of neuroendocrine marker expression in Leydig cells of adult rats. Repr Dom Anim 2006; 41: 204-209.

Foster K, Sheridan J, Veiga-Fernandes H, Roderick K, Pachnis V, Adams R, et al. Contribution of neural crest-derived cells in the embryonic and adult thymus. J Immunol 2008; 180: 3183-3189. DOI: 10.4049/jimmunol. 180.5.3183

Gong Y-G, Feng M-M, Hu X-N, Wang Y-Q, Gu M, Zhang W, et al. Peptidergic not monoaminergic fibers profusely innervate the young adult human testis. J Anat 2009; 214: 330-338. DOI: 10.1111/j.1469-7580.2008.01038.x

Makala H, Pothana L, Sonam S, Malla A, Goel S. Regeneration of Leydig cells in ectopically autografted adult mouse testis. Reproduction 2015; 149: 259-268. DOI: 10.1530/REP-14-0576

Benton L, Shan L-X, Hardy MP. Differentiation of adult Leydig cells. J Steroid Biochem Mol Biol 1995; 53: 61-68.

Ge R-S, Dong Q, Sottas CM, Papadopoulos V, Zirkin BR, Hardy MP. In search of rat stem Leydig cells: identification, isolation, and lineage-specific development. Proc Natl Acad Sci USA 2006; 103: 2719-2724. DOI: 10.1073/pnas.0507692103

Tang H, Brennan J, Karl J, Hamada Y, Raetzman L, Capel B. Notch signaling maintains Leydig progenitor cells in the mouse testis. Development 2008; 135:3745-3753. DOI: 10.1242/dev.024786

Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 2011; 21: 193-215. DOI: 10.1016/j.devcel.2011.07.001

Davidoff MS, Middendorff R, Enikolopov G, Rietmacher D, Holstein AF, Müller D. Progenitor cells of the testosterone-producing Leydig cells revealed. J Cell Biol 2004; 167: 935-944. DOI: 10.1083/jcb.200409107

Davidoff MS, Middendorff R, Müller D, Holstein AF. The Neuroendocrine Leydig Cells and their Stem Cell Progenitors, the Pericytes. Adv Anat Embryol Cell Biol 2009; 205: 1-154. DOI: 10.1007/978-3-642-00513-8

da Silva Meirelles L, Chagastellesd PC, Nardi NB. Mesenchymal stem cells reside in virtually all postnatal organs and tissues. J Cell Sci 2006; 119: 2204-2213. DOI: 10.1242/jcs.02932

Pacini S, Petrini I. Are MSCs angiogenic cells? New insights on human nestin-positive bone-marrow-derived multipotent cells. Front Cell Dev Biol 2014; 2, Article 20. DOI: 10.3389/fcell.2014.00020. eCollection 2014

Liu C, Rodriguez K, Yao HH. Mapping lineage progression of somatic progenitor cells in the mouse fetal testis. Development 2016; 143: 3700-3710. DOI: 10.1242/dev.135756

Chen H, Wang Y, Ge R, Zirkin BR. Leydig stem cells: identification, proliferation and differentiation. Mol Cell Endocrinol 2017; 445: 65-71. DOI: 10.1016/j.mce.2016.10.010.

Ye L, Li X, Li L, Chen H, Ge R-S. Insights into the development of the adult Leydig cell lineage from stem Leydig cells. Front Physiol 2017; 8:430. DOI: 10.3389/ fphys.2017.00430

Zwaka TP, Thomson JA. A germ cell origin of embryonic stem cells? Development 2005; 132: 227-233. DOI: 10.1242/dev.01586

Crisan M, Yap S, Casteilla L, Chen C-W, Corselli M, Park TS, Andriolo G, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3: 301–313. DOI: 10.1016/J. Stem.2008.07.003

De-Miguel MP, Fuentis-Julian S, Alcaina Y. Pluripotent stem cells: origin, maintenance and induction. Stem Cell Rev and Rep 2010; 6: 633- 6409. DOI: 10.1007/ s12015-010-9170-1

Collas P. Programming differentiation potential in mesenchymal stem cells. Epigenetics 2010; 5: 476-482. DOI: 10.4161/epi.5.6.12517

Dore-Duffy P. Pericytes: pluripotent cells of the blood brain barrier. Curr Pharm Des 2008; 14:1581-1593. DOI: 10.2174/138161208784705469

Caplan P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cells 2008; 2:313-319. DOI: 10.1016/j.stem.2008.03.002.

Caplan AI. All MSCs are pericytes? Cell Stem Cell 2008; 3:229-230. DOI: 10.1016/J.Stem.2008.08.008

Chen H, Ge R-S, Zirkin BR. Leydig cells: From stem cells to aging. Mol Cell Endocrinol 2009; 306: 9-16. DOI:10.1016/j.mce.2009.01.023

Péault B. Are mural cells guardians of stemness? From pluri- to multipotency via vascular pericytes. Circulation 2012; 125:12-13. DOI: 10.1161/CIRCULATIONAHA.111.073445

Özen I, Boix J, Paul G. Perivascular mesenchymal stem cells in the adult human brain: a future target for neuroregeneration? Clin Translat Med 2012; 1(1):30. DOI: 10.1186/2001-1326-1-30.

Kucia M, Wu W, Ratajczak MZ. Bone marrow-derived very small embryonic-like stem cells: their developmental origin and biological significance. Dev Dynam 2007; 236:3309-3320. DOI: 10.1002/dvdy.21180

Kucia M, Wysoczynski M, Ratajczak J, Ratajczak MZ. Identification of very small embryonic like (VSEL) stem cells in bone marrow. Cell Tiss Res 2008; 331:125-134. DOI: 10.1007/s00441-007-0485-4

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

Dore-Duffy P, Katychev A, Wang X, Buren EV.. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cerebral Blood Flow Metab 2006; 26:613-624. DOI: 10.1038/Sj.Jcbfm.9600272

Dore-Duffy P, Mehedi A, Wang X, Bradley M, Trotter R, Gow A. Immortalized CNS pericytes are quiescent smooth muscle actin-negative and pluripotent. Microvasc Res 2011; 82: 18-27. DOI:10.1016/j.mvr.2011.04.003

Suwinska A, Ciemerych MA. Factors regulating pluripotency and differentiation in early mammalian embryos and embryo-derived stem cells. Vitamins and Hormones 2011; 87: 1-37 DOI: 10.1016/B978-0-12-386015- 6.00022-6

Kucia M, Machalinski B, Ratajczak MZ. The developmental deposition of epiblast/germ cell-line derived cells in various organs as a hypothetical explanation of stem cell plasticity? Acta Neurobiol Exp 2006; 66:331–341

Ratajczak MZ, Zuba-Surma EK, Wysoczynski M, Ratajczak J, Kucia. Very small embryonic-like stem cells: Characterization, developmental origin, and biological significance. Exp Hematol 2008; 36: 742-751. DOI: 10.1016/j.exphem.2008.03.010

Ratajczak MZ, Shin D-M, Liu R, Mierzeiewska K, Ratajczak J, Kucia M, et al. 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 2012; 4: 235-246. DOI: 10.18632/aging.100449

Ratajczak MZ, Zuba-Surma E, Kucia M, Poniewierska A, Suszynska M, Ratajczak J. Pluripotent and multipotent stem cells in adult tissues. Adv Med Sci 2012; 57: 1-17. DOI: 10.2478/v10039-012-0020-z

Montiel-Eulefi E, Sánchez R, Rojas M, Bustos-Obregon E. Epiblast embryo stem cells give origin to adult pluripotent cell populations: primordial germ cell, pericytic and haematopoietic stem cells. A review. Int J Morphol 2009; 27: 1325-1333

De-Miguel MP, Arnalich-Montiel F, Lopez-Iglesias P, Blasquez-Martinez A, Nistal M. Epiblast-derived stem cells in embryonic and adult tissues. Int J Dev Biol 2009; 53:1529-1540. DOI: 10.1387/ijdb.072413md

Suwinska A, Czolowska R, Ozdzenski W, Trakowski AK. Blastomeres of the mouse embryo lose totipotency after the fifth cleavage division: Expression of Cdx2 and Oct4 and developmental potential of inner and outer blastomeres of 16- and 32-cell embryos. Dev Biol 2008; 322:133-144. DOI:10.1016/j.ydbio.2008.07.019

Shan L-X, Hardy MP. Developmental changes in levels of luteinizing hormone receptor and androgen receptor in rat Leydig cells. Endocrinology 1992; 131:1107-1114.

Hardy MP, Zirkin BR, Ewing LL Kinetic studies on the development of the adult population of Leydig cells in testes of the pubertal rat. Endocrinology 1989; 124:762-770

Chemes HE. Leydig cell development in humans. In: Payne, AH, Hardy MP, Russell LD (Eds.), The Leydig Cell. Cache River Press, 1996; Vienna, IL, pp. 175–201

Etchevers HC, Vincent C, Le Douarin NM, Couly GF. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 2001; 128:1059-1068

Guillemin GJ, Brew BJ (2004) Microglia, macrophages perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol 75: 388-397. DOI: 10.1189/jlb.0303114

Trost A, Lange S, Schroedl F, Bruckner D, Motloch KA, Bogner B, et al. Brain and retinal pericytes: origin, function and role. Front Cell Neurosci 2016; 10:20. DOI: 10.3389/fncel.2016.00020

Sá-Pereira I, Brites D, Brito MA. Neurovascular unit: a focus on pericytes. Mol Neurobiol 2012; 45:327-347 DOI: 10.1007/s12035-012-8244-2

Rhodin JAG, Fujita H. Capillary growth in the mesentery of normal young rats. Intravital video and electron microscope analyses. J Submicrosc Cytol Pathol 1989; 21:1–34

Diaz-Flores L Jr, Madrid JF, Guitérrez R. Adult stem and transit-amplifying cell location. Histol Histopathol 2006; 21:995-1027. DOI: 10.14670/HH-21.995

Diaz-Flores L, Gutiérrez R, Madrid JF, Varela H, Valladares F, Acosta E, et al. Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 2009; 24: 909-969. DOI: 10.14670/HH-24.909

Mancini RF, Vilar O, Lavieri JC, Andrada JA, Heinrich JJ. Development of Leydig cells in the normal human testis: A cytological, cytochemical and quantitative study. Am J Anat 1963; 112: 203-214. DOI: 10.1002/aja.1001120206

Russell LD, de Franca LR. Building a testis. Tissue Cell 1995; 27: 129-147. DOI:10.1016/S0040-

(95)80016-6

Haider SG , Laue D , Schwochau G , Hilscher B. Morphological studies on the origin of adult-type Leydig cells in rat testis. Ital J Anat Embryol 1995; 100 (Suppl 1): 535 – 541

Haider SG. Leydig cell steroidogenesis: unmasking the functional importance of mitochondria. Endocrinology 2007; 148: 2581–2582. DOI: 10.1210/en.2007-0330

Chemes HE. Leydig cell development in humans. In: Payne, AH, Hardy MP, Russell LD (Eds.), The Leydig Cell. Cache River Press, Vienna, IL, 1996; pp. 175–201

Kilcoyne KR, Smith LB, Atanassova N, Macpherson S, McKinell C, van den Driesche S, et al. Fetal programming of adult Leydig cell function by androgenic effects on stem/progenitor cells. Proc Natl Acad Sci USA 2014; 111: E1924-E1932. DOI: 10.1073/pnas.1320735111

Fecteau KA, Markonjich L, Mason JI, Mendis-Handagama SMLC. Detection of platelet-derived growth factor-α (PDGF-A) protein in cells of Leydig lineage in the postnatal rat testis. Histol Histopathol 2006; 21: 1295-1302. DOI: 10.14670/HH-21.1295.

Svingen T, Koopman P. Building the mammalian testis: origins, differentiation, and assembly of the component cell populations. Genes Dev 2013; 27: 2409-2426. DOI: 10.1101/gad.228080.113.

Kerr JB, Bartlett JMC, Donachie K, Sharpe RM. Origin of regenerating Leydig cells in the testis of adult rat. An ultrastructural, morphometric and hormonal study. Cell Tissue Res 1987; 249: 367-377. DOI: 10.1007/BF00215521

Nehls V, Denzer K, Drenckhahn D. Pericyte involvement in capillary sprouting during angiogenesis in situ. Cell Tissue Res 1992; 270: 469-474. DOI: 10.1007/BF00645048

Haider SG, Servos G. Ultracytochemistry of 3ß-hydroxysteroid dehydrogenase in Leydig cell precursors and vascular endothelial cells of the postnatal rat testis. Anat Embryol 1998: 198: 101-110. DOI: 10.1007/s004290050168

Haider SG, Servos K, Tran N. 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 Inc. Totowa, NJ, 2007; pp. 33-45

Ariyaratne HB , Mendis-Handagama SMLC. Changes in the testis interstitium of Sprague Dawley rats from birth to sexual maturity. Biol Reprod 2000; 62: 680-690. DOI: 10.1095/biolreprod62.3.680

Allt G, Lawrenson JG Pericytes: cell biology and pathology. Cell Tiss Organs 2001; 169: 1-11. DOI: 10.1159/000047855

O’Shaughnessy PJ, Hu I, Baker PJ. Effect of germ cell depletion on levels of specific mRNA transcripts in mouse Sertoli cells and Leydig cells. Reproduction 2008; 135: 839-850. DOI: 10.1530/REP-08-0012

Stanley E, Lin C-Y, Jin S, Liu J, Sottas CM, Ge R et al. Identification, prtoliferation, and differentiation of adult Leydig stem cells. Endocrinology 2012; 153: 5002-5010. https://doi.org/10.1210/en.2012-1417

Landreh L, Stukenborg J-B, Söder O, Svechnikov K Phenotype and steroidogenic potential of

PDGFα-positive rat neonatal peritubular cells. Mol Cell Endocrinol 2013; 372: 96-104. DOI: 10.1016/j.mce.2013.03.019

Landreh L, Spinner K, Schubert K, Häkkinen MR, Auriola S, Poutanern M, et al. Human testicular peritubular cells host putative stem Leydig cells with steroidogenic capacity. J Clin Endocrinol Metab 2014; DOI: 10.1210/jc.2013-4199

Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre-recombinase. Curr Biol 1998; 8: 1323–1326. DOI: 10.1016/s0960-9822(07)00562-3

Etchevers HC, Vincent C, Le Douarin NM, Couly GF. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 2001; 128: 1059-1068.

Korn J, Christ B, Kurz H. Neuroectodermal origin of brain pericytes and vascular smooth muscle cells. J Comp Neurol 2002; 442: 78-88. DOI: 10.1002/cne.1423

Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, et al. Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci USA 1995; 92:11879–11883

Müller SM, Stolt CC, Terswzowski G, Blum C, Amaqgai T, Kessaris N, Innarelli P, et al. Neural crest origin of perivascular mesenchyme in the adult thymus. J Immunol 2008; 180: 5344-5351.

Simon C, Lickert H, Götz M, Dimou L. Sox10-iCre-ERT2: a mouse line to inducibly trace the neural crest and oligodendrocyte lineage. Genesis 2011; 50: 506-515. DOI: 10.1002/dvg.22003

Trost A, Schroedl F, Lange S, Rivera FJ, Tempfer H, Korntner S et al. Neural crest origin of retinal and choroidal pericytes. Invest Ophthalmol Vis Sci 2013; 54: 7910-7921. DOI:10.1167/iovs.13-12946

Ergün S, Tilki D, Klein D.Vascular wall as a reservoir for different types of stem and progenitor cells. Antiox Redox Signal 2011; 15: 981-995. DOI: 10.1089/ars.2010.3507

Corselli M, Chen C-W, Sun B, Yap S, Rubin JP, Péault B. The tunica adventitia of human arteries and veins as a source of mesenchymal stem cells. Stem Cells Dev 2012; 21: 1299-1308. DOI: 10.1089/scd.2011.0200

Chen Q, Zhang H, Liu Y, Adams S, Eilken H, Stehling M, et al. Endothelial cells are progenitors of cardiac pericytes and vascular smooth muscle cells. Nat Commun 2016; 7:12422. DOI: 10.1038/ncomms12422

Ozerdem U, Alitalo K, Salven P, Andrew L. Contribution of bone marrow-derived pericyte precursor cells to corneal vasculogenesis. Invest Ophthalmol Vis Sci 2005; 46:3502–3506. DOI:10.1167/iovs.05-0309

Pfister F, Przybyt E, Harmsen MC, Hammes H-P. Pericytes in the eye. Pflüg Arch –Eur J Physiol 2013; 465: 789-796. DOI 10.1007/s00424-013-1272-6

Brennan J, Tilmann C, Capel B. PDGFR-α mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 2003; 17: 800-810. DOI:10.1101/gad.1052503

Jackson AE , O’Leary PC , Ayers MM , de Kretser DM. The effects of ethylene dimethane sulphonate (EDS) on rat Leydig cells: evidence to support a connective tissue origin of Leydig cells. Biol Reprod 1986; 35: 425-437. DOI: 10.1095/biolreprod35.2.425

Jegou B , Pineau C. Current aspects of autocrine and paracrine regulation of spermatogenesis. In: Mukhopadhyay AK , Raizada MK (Eds), Tissue Renin-Angiotensin Systems. Current Concepts of Local Regulators in Reproductive and Endocrine Organs. Plenum Press, New York 1995; pp 67 – 86

Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 2004; 304: 1338-1340. DOI: 10.1126/science.1095505

Ergün S, Stingl J, Holstein AF. Microvasculature of the human testis in correlation to Leydig cells and seminiferous tubules. Andrologia 1994; 26:255-62. DOI: 10.1111/j.1439-0272.1994.tb00799.x

Flamme I, Frölich T, Risau W. Molecular mechanisms of vasculogenesis and embryonic angiogenesis. J Cell Physiol 1997; 173: 206-210. DOI: 10.1002/(SICI)1097-4652(199711)173:2<206::AID-JCP22>3.0.CO;2-C

Nikolova G, Lammert E. Interdependent development of blood vessels and organs. Cell Tissue Res 2003; 314: 33-42. DOI: 10.1007/s00441-003-0739-8

Chappell JC, Bautch VL.Vascular development: genetic mechanisms and links to vascular disease. Curr Top Dev Biol 2010; 90: 43-72. DOI 10.1016/S0070-2153(10)90002-1

Weerasooriya TR, Yamamoto T. Three-dimensional organization of the vasculature of the rat spermatic cord and testis. Cell Tissue Res 1985; 241: 317-323 DOI: 10.1007/BF00217176

Murakami T, Uno Y, Ohtsuka A, Taguchi T. 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 1989; 52: 151-172. DOI: 10.1679/aohc.52.151

Suzuki F, Nagano T. Microvasculature of the human testis and excurrent duct system. Resin-casting and scanning electron-microscopic studies. Cell Tissue Res 1986; 243: 79-89. DOI: 10.1007/BF00221855

Javaherian A, Kriegstein A. A stem cell niche for intermediate progenitor cells of the embryonic cortex. Cerebral Cortex 2009; 19: i70-i77. DOI: 10.1093/cercor/bhp029.

Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000; 425: 479-494. DOI: 10.1002/1096-9861(20001002)425:4<479::AIDCNE2> 3.0.CO;2-3

Brennan J, Karl J, Capel B. Divergent vascular mechanisms downstream of Sry establish the arterial system in the XY gonad. Dev Biol 2002; 244: 418-428. DOI:10.1006/dbio.2002.0578

Combes AN, Wilhelm D, Davidson T, Dejana E, Harley V, Sinclair A et al. Endothelial cell migration directs testis cord formation. Developmental Biology 2009; 326: 112–120 DOI:10.1016/j.ydbio.2008.10.040

Ergün S, Davidoff M, Holstein AF. Capillaries in the lamina propria of human seminiferous tubules are partly fenestrated. Cell Tissue Res 1996; 286: 93-102. DOI: 10.1007/s004410050678

Ergün S, Harneit S, Paust HJ, Mukhopadhyay AK, Holstein AF. Endothelin and endothelin receptors A and B in the human testis. Anat Embryol 1999; 199: 207-214.

da Silva Meirelles L, Caplan AI, Nardi NB. Pericytes as the source of mesenchymal stem cells. In: dos Santos Goldenberg RC, Campos de Carvalho AC (Eds) Resident Stem Cells and Regenerative Therapy 2013; pp. 233-250. Elsevier Inc. DOI:10.1016/B978-0-12-416012-5.00012-8

Karow M. Mountaineering pericytes - A universal key to tissue repair? Bioassays 2013; 35: 771-774. DOI: 10.1002/bies.201300055

Joseph NM, Mukouyama YS, Mosher JT, Jaegle M, Crone SA, Dormand EL, et al. Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneural fibroblasts in addition to Schwann cells. Development 2004; 131: 5599-5612. DOI: 10.1242/dev.01429

Petrini M, Pacini S, Trombi L, Fazzi R, Montali M, Ikehara S, et al. Identification and purification of mesodermal progenitor cells from human adult bone marrow. Stem Cells Dev 2009; 18: 857–866. DOI:10.1089/scd.2008.029.

Pacini S, Carnicelli V, Trombi L, Montali M, Fazzi R, Lazzarini E, et al. Constitutive expression of pluripotency-associated genes in Mesodermal Progenitor Cells (MPCs). PLoS ONE 2010; 5:e9861. DOI: 10.1371/journal.pone.0009861

Buehr M, Smith A. Genesis of embryonic stem cells. Phil Trans R Soc Lond B 2003; 358: 1397-1402. DOI: 10.1098/rstb.2003.1327

Rossant J. Stem cells from the mammalian blastocyst. Stem Cells 2001; 19: 477-482. DOI: 10.1634/stemcells.19-6-477

Smith, A. G. Embryo-derived stem cells: of mice and men. Ann Rev Cell Devl Biol 2001; 17: 435–462. DOI: 10.1146/annurev.cellbio.17.1.435

Li L, Xie T. Stem cell niche: Structure and function. Annu Rev Cell Dev Biol 2005; 21: 605–631. DOI: 10.1146/annurev.cellbio.21.012704.131525

ChenY-T, Chang F-C, Wu C-F, Chou Y-H, Hsu H-L, Chiang W-C, et al. Platelet-derived growth factor receptor signaling activates pericyte-myofibroblast transition in obstructive and post-ischemic kidney fibrosis. Kidney Intern 2011; 80: 1170-1181. DOI:10.1038/ki.2011.208

Javaherian A, Kriegstein A. A stem cell niche for intermediate progenitor cells of the embryonic cortex. Cerebral Cortex 2009; 19: i70-i77. DOI: 10.1093/cercor/bhp029.

Rompolas P, Mesa KR, Greco V. Spatial organization within a niche as a determinant of stem-cell fate. Nature 2013; 502: 513-518. DOI:10.1038/nature12602

Iglesias-Bartolome R, Gutkind JS. Keeping the epidermal stem cell niche in shape. Cell Stem Cells 2010; 7:143-145. DOI: 10.1016/j.stem.2010.07.008

Caplan AI. Mesenchymal stem cells. J Orthop Res 1991; 9: 641-650.

de Souza LEB, Malta TM, Kashima HS, Covas DT. Mesenchymal stem cells and pericytes: To what extent are they related? Stem Cells and Development. 2016; 25(24): 1843-1852. https://doi.org/10.1089/scd.2016.0109

Lin C-S, Xin Z-C, Deng C-H, Ning H, Lin G, Lue T F. Defining adipose tissue-derived stem cells in tissue and in culture. Histol Histopathol 2010; 25: 807-815. DOI:10.14670/HH-25.807.

Bouacida A, Rosset P, Trichet V, Guilloton F, Espagnolle N, Cordonier T, et al. Pericyte-like progenitors show high immaturity and engraftment potential as compared with mesenchymal stem cells. PLoS ONE 2012; 7(11): e486548. DOI: 10.137/journal.pone.0048648

Mendes-Jorge L, Llombart C, Ramos D, López-Luppo M, Valença A, Nacher V, et al. Intercapillary bridging cells: Immunocytochemical characteristics of cells that connect blood vessels in the retina. Exp Eye Res 2012; 98: 79-82. DOI:10.1016/j.exer.2012.03.010

Gökçinar-Yagei B, Uçkan-Çetinkaya, Çelebi-Saltik B. Pericytes: Properties, functions and applications in tissue engineering. Stem Cell Rev Rep 2015; 11: 549-559. DOI: 10.1007/s12015-015-9590-z

Guimarães-Camboa N, Cattaneo P, Sun Y, Moore-Morris T, Gu Y, Dalton ND, et al. Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell 2017; 20: 345-359. DOI.org/10.1016/j.stem.2016.12.006

Cano E, Gebala V, Gerhardt H. Pericytes or mesenchymal sdtem cells: Is that the question? Cell Stem Cell 2017; 20: 296-297. DOI: /10.1016/j.stem.2017.02.005

Lindner U, Kramer J, Rohwedel J, Schlenke P. Mesenchymal stem or stromal cells: Toward a better understanding of their biology? Transfus Med Hemother 2010; 37: 75-83. DOI: 10.1159/000290897

Zimmerlin L, Donnenberg VS, Pfeifer ME, Meyer EM, Péault B, Rubin JP, et al. Stromal vascular progenitors in adult human adipose tissue. Cytometry Part A 2010; 77A: 22-30. DOI: 10.1002/cyto.a.20813

Zimmerlin L, Donnenberg VS, Donnenberg AD, Pericytes: A universal adult tissue stem

Murray IR, West CC, Hardy WR, James AW, Park TS, Nguyen A et al. Natural history of mesenchymal stem cells, from vessel walls to culture vessels. Cell Mol Life Sci 2013; DOI 10.1007/s00018-013-1462-6

Dar A, Domev H, Ben-Yosef O, Tzukerman M, Zeevi-Levin N, Novak A, et al. Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation 2012; 125: 87-99. DOI: 10.1161/CIRCULATIONAHA. 111.048264

Rowley JE, Johnson JR. Pericytes in chronic lung disease. Int Arch Allergy Immunol 2014; 164:178–188. DOI: 10.1159/000365051

Tosh D, Slack JMW. How cells change their phenotype. Nature Rev 2002; 3: 187-194. DOI: 10.1038/nrm761

Shen CC, Kang Y-H, Yu L, Cui D-d, He Y, Yang J-L, Gou L-T. Human testis-expressed sequence 101 is limitedly distributed in germinal epithelium of testis and disappears in seminoma. Biol Res 2014; 47: 52. DOI:10.1186/0717-6287-47-52

Murasawa S, Kawamoto A, Horii M, Nakamori S, Asahara T. Niche-dependent translineage commitment of endothelial progenitor cells, not cell fusion in general, into myocardial lineage cells. Arterioscler Thromb Vasc Biol 2005; 25:1388-1394 DOI: 10.1161/01.

ATV.0000168409.69960.e9

Song L, Tuan RS. Transdifferentiation po ã q q -tential of human mesenchymal stem cells derived

from bone marrow. FASEB J 2004; 18: 980-982. DOI: 10.1096/fj.03-1100fje

Song L, Webb NE, Song Y, Tuan RS. Identification and functional analysis of candidate genes regulating mesenchymal stem cell self-renewal and multipotency. Stem Cells 2006; 24: 1707-1718. DOI: 10.1634/stemcells.2005-0604

Bianco P, Cossu G. Uno, nessuno e centomila: Searching for the identity of mesodermal progenitors. Exp Cell Res 1999; 251: 257-263. DOI: 10.1006/excr.1999.4592

De Angelis L, Berghella L, Coletta M, Lattanzi L, Zanchi M, Gabriella Cusella-De Angelis M, et al. Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J Cell Biol 1999; 147: 869-877. DOI: 10.1083/jcb.147.4.869

Minasi MG, Riminussi M, De Angelis L, Borello U, Berarducci B, Innocenzi A, et al. The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 2002; 129: 2773-2783.

Lin S-L, Kisseleva T, Brenner DA, Jeremy S. Duffield JS. Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 2008; 173: 1617-1627. DOI: 10.2353/ajpath.2008.080433

Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenancxe throughout life. Cell 2008; 132: 598-611. DOI 10.1016/j.cell.2008.01.038

Rao M. Stem and precursor cells in the nervous system. J Neurotrauma 2004; 21(4): 415–427. DOI: 10.1089/089771504323004566

Tavian M, Zheng B, Oberlin E, Crisan M, Sun B, Huard J, et al. The vascular wall as a source of stem cells. Ann NY Acad Sci 2005; 1044: 41-50. DOI: 10.1196/annals. 1349.006

Ge R-S, Dong Q, Sottas CM, Chen H, Zirkin BR, Hardy MP. Gene expression in rat Leydig cells during development from the progenitor to adult stage: a cluster analysis. Biol Reprod 2005; 72: 1405-1415. DOI: 10.1095/biolreprod.104.037499

Teerds K, Rijntjes E. Dynamics of Leydig cell regeneration after EDS. A model for postnatal Leydig cell development. In: Payne AH, Hardy MP (Eds), Contemporarry Endocrinology: The Leydig Cell in Health and Disease Humana Press Inc, Totowa, NJ, 2007; pp 91-116

Lin C-S, Lue TF. Defining vascular stem cells. Stem Cells Dev 2013; 22: 1018–1026. DOI:10.1089/scd.2012.0504

Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968; 6, 230–247. DOI: 10.1097/00007890-196803000-00009

Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok V. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 1974; 14: 331-340.

Horwitz EM, Le BK, Dominici M, Zetterberg E, Ringdén O. Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy 2005; 7: 393–395. DOI: 10.1080/14653240500319234

Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini FC, Krause DS. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8:315-317. DOI: 10.1080/14653240600855905

Lamagna C, Bergers G. The bone marrow constitutes a reservoir of pericyte progenitors. J Leukoc Biol 2006; 80: 677-681. DOI: 10.1189/jlb.0506309

Bexell D, Gunnarsson S, Tormin A, Darabi A, Gisselsson D, Roybon L. Bone marrow multipotent mesenchymal stroma cells act as pericyte-like migratory vehicles in experimental gliomas. Mol Ther 2009; 17:183-190. DOI:10.1038/mt.2008.229

Nakagomi T, Kubo S, Nakano-Doi A, Sakuma R, Lu S, Narita A. Brain vascular pericytes following ischemia have multipotential stem cell activity to differentiate into neural and vascular lineage cells. Stem Cells 2015; 33: 1962-1974 DOI 10.1002/stem.1977

Zouani OF, Lei Y, Durrieu M-C. Pericytes, stem-celllike cells, but not mesenchymal stem cells are recruited to support microvascular tube stabilization. Small 2013; 9: 3070-3075. DOI: 10.1002/smll.201300124

Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cells 2008; 2: 313-319. DOI: 10.1016/j.stem.2008.03.002.

Friedrich R, Holstein AF, Middendorff R, Davidoff MS. Vascular wall cells contribute to tumorigenesis in cutaneous neurofibromas of patients with neurofibromatosis type 1. A comparative histological, ultrastructural and immunohistochemical study. Anticancer Res 2012;

: 2139-2158

Göritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisén J. A pericyte origin of spinal cord scar tissue. Science 2011; 333: 238-242.

Tempel ZJ, Monaco EA III, Friedlander RM. Pericytes as a therapeutic target in scar formation after spinal cord injury. Science 2013; 73: N18-N20.

Kokovay E, Li L, Cunningham LA. Angiogenic recruitment of pericytes from bone marrow after stroke. J Cerebral Blood Flow Metabol 2006; 26: 545-555. DOI:10.1038/sj.jcbfm.9600214

Haider SG. Cell biology of Leydig cells in the testis. Int Rev Cytol 2004; 233: 181–241. DOI: 10.1016/S0074-7696(04)33005-6

Ariyaratne HB , Mendis-Handagama SMLC. Changes in the testis interstitium of Sprague Dawley rats from birth to sexual maturity. Biol Reprod 2000; 62: 680 –690. https://doi.org/10.1095/biolreprod62.3.680

Shen Q, Wang W, Kokovay E, Lin G, Chang S-M, Goderie SK, et al. Adult ZVZ stem cells lie in a vascular niche: a quanitative analysis of niche-cell interactions. Cell Stem Cell 2008; 3: 289-300. DOI: 10.1016/j.stem.2008.07.025

Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 2004; 304: 1338-1340. DOI: 10.1126/science.1095505

McCarty JH. Cell biology of the neurovascular unit: implications for drug delivery across the blood-brain barrier. ASSAY Drug Dev Technol 2005; 3: 89-95. DOI:10.1089/adt.2005.3.89

McCarty JH. Cell adhesion and signaling networks in brain neurovascular units. Curr Opinion Hematol 2009; 16: 209-214.

Sá-Pereira I, Brites D, Brito MA. Neurovascular unit: a focus on pericytes. Mol Neurobiol 2012; 45: 327-347. DOI: 10.1007/s12035-012-8244-2

Itoh Y, Toriumi H, Yamada S, Hoshino H, Suzuki N. Astrocytes and pericytes cooperatively maintain a capillary-like structure composed of endothelial cells on gel matrix. Brain Res 2011; 1406: 74-83. DOI:10.1016/j.brainres.2011.06.039

Alvarez-Buylla A, Seri B, Doetsch F. Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 2002; 57: 751-758. DOI: 10.1016/S0361-9230(01)00770-5

Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang L-P. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 2003; 23: 373-382. DOI: 10.1016/S1044-7431(03)00060-5

Hill WD, Hess DC, Martin-Studdard A, Carotheres J J, Zheng J, Hale D, et al. SDF-1 (CXCL12) is upregulated in the ischemic penumbra following stroke: association with bone marrow cell homing to injury. J Neuropathol Exp Neurol 2004; 63: 84-96. DOI: 10.1093/jnen/63.1.84

Sild M, Rithazer ES. Radial glía: progenitor, pathway, and partner. Neuroscience 2011; 17: 288-302. DOI: 10.1177/1073858410385870

Gonzalez-Perez O. Neural stem cells in the adult human brain. Biol Biomed Rep 2012; 2(1) 59-69. DOI:10.1155/2012/378356

Jiang Y, Hernderson D, Blackstad M, Chen A, Miller RF, Verfaillie CM. Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc Natl Acad Sci USA 2003; 100: 11854-11860. DOI: 10.1073/pnas.1834196100

Morshead CM. Adult neural stem cells: attempting to solve the identity crisis. Dev Neurosci 2004; 26: 93-199. DOI: 10.1159/000082130

Wei LC, Shi M, Chen LW, Cao R, Zhang P, Chan YS. Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Dev Brain Res 2002; 139: 9-17. PII: S0165-3806(02)00509-6

Zhu X, Bergles DE, Nishiyama A. NG2 cells generate both oligodendrogcytes and gray matter astrocytes. Development 2008; 135: 145-157. DOI:10.1242/dev.004895

Hara Y, Nomura T, Yoshizaki K, Frisén J, Osumi N. Impaired hippocampal neurogenesis and vascular formation in ephrin-A5-deficient mice. Stem Cells 2010; 28:974–983. DOI: 10.1002/stem.427

Angelova P, Davidoff MS. Immunocytochemical demonstration of substance P in hamster Leydig cells during ontogenesis. Z Mikrosk Anat Forsch 1989; 103: 560 – 566.

Doetsch F. The glial identity of neural stem cells. Nat Neurosci 2003; 6: 1127-1134. DOI: 10.1038/nn1144

Angelova P, Davidoff MS , Baleva K, Staykova M. Substance P and neuron-specific enolase-like immunoreactivity of rodent Leydig cells in tissue section and cell culture. Acta Histochem 1991: 91: 131-139. DOI: 10.1016/S0065-1281(11)80266-7

Chiwakata C, Brackmann B, Hunt N, Davidoff M, Schulze W, Ivell R. Tachykinin (Substance P) gene expression in Leydig cells of the human and mouse testis. Endocrinology 1991; 128: 2441–1448. DOI: 10.1210/endo-128-5-2441

Davidoff MS , Middendorff R , Koeva Y , Pusch W, Jezek D , Muller D. 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 2001; 106 (Suppl 2): 173–180.

Middendorff R , Davidoff MS , Holstein AF. Neuroendocrine marker substances in human Leydig cells – changes by disturbances of testicular function. Andrologia 1993; 25: 257–262. DOI: 10.1111/j.1439-0272.1993.tb02722.x

Le Douarin NM, Dupin E. Multipotentiality of the neural crest. Curr Opin Genet Dev 2003; 13: 529-536. https://doi.org/10.1016/j.gde.2003.08.002

Barembaum M, Bronner-Fraser M. Early steps in neural crest specification. Seminars Cell Dev Biol 2005; 16: 642-646. DOI: 10.1016/j.semcdb.2005.06.006

Weston JA, Thiery JP. Pentimento: Neural crest and the origin of mesectoderm. Dev Biol 2015; 401: 37-61. DOI.org/10.1016/j.ydbio.2014.12.035

Weston J A, Yoshida H, Robinson V, Nishikawa S, Fraser ST, Nishikawa S. Neural crest and the origin of ectomesenchyme: neural fold heterogeneity suggests an alternative hypothesis. Dev Dyn 2004; 229: 118-130. DOI 10.1002/dvdy.10478

Breau MA, Pietri T, Stemmler MP, Thiery P, Weston JA. A nonneural epithelial domain of embryonic cranial neural folds gives rise to ectomesenchyme. Proc Natl Acad Sci USA 2008; 105: 7750-7755. DOI: 10.1073pnas.0711344105

Trainor PA, Melton KR, Manzanares M. Origins and plasticity of neural crest cells and their roles in jaw and craniofacial evolution. Int J Dev Biol 2003; 47: 541-553

Trainor PA. Spezification and pattering of neural crest cells during craniofacial development. Brain Behav Evol 2005; 66: 266-280. DOI: 10.1159/000088130

Crane JF, Trainor PA. Neural crest stem and progenitor cells. Ann Rev Dev Biol 2006; 22: 267-286. DOI: 10.1146/annurev.cellbio.22.010305.103814

Kojima Y, Kaufman-Francis K, Studdert JB, Steiner KA, Power MD, Loebel DAF et al. The transcriptional and functional properties of mouse epiblast stem cells resemble the anterior primitive streak. Cell Stem Cell 2014;14:107-120. DOI: 10.1016/j.stem.2013.09.014

Griswold SL, Behringer RR. Fetal Leydig cell origin and development. Sex Dev 2009; 3:1–15. DOI: 10.1159/000200077

Tam PP, Loebel DA. Gene function in mouse embryogenesis: get set for gastrulation. Nat Rev Genet 2007; 8:368-381. DOI: 10.1038/nrg2084

Pauklin S, Pedersen RA, Vallier L. Mouse pluripotent stem cells at a glance. J Cell Sci 2011; 124: 3727-3732. DOI:10.1242/jcs.074120

Lee RTH, Negai H, Nakaya Y, Sheng G, Trainor PA, Weston JA. Cell delamination in the mesencephalic neural fold and its implication for the origin of ectomesenchyme. Development 2013; 140: 4890-4902. DOI:10.1242/dev.094680

Donoghue PCJ, Graham A, Kelsh RN. The origin and evolution of the neural crest. Bioessays 2008; 30: 530-541. DOI:10.1002/bies.20767.

Nichols DH. Formation and distribution of neural crest mesenchyme to the first pharyngeal arch region of the mouse embryo. Am J Anat 1986; 176:221–231.

Nichols DH. Neural crest formation in the head of the mouse embryo as observed using a new histological technique. J Embryol Exp Morph 1981; 64:105-120.

Spence SG, Poole TJ. Developing blood vessels and associated extracellular matrix as substrates for neural crest migration in Japanese quail, Coturnix coturnix japonica. Int J Dev Biol 1994; 38: 85-98.

Maekawa M, Kamimura K, Nagano T. Peritubular myoid cells in the testis: their structure and function. Arch Histol Cytol 1996; 59: 1-13

Ge R-S, Dong Q, Sottas CM, Papadopoulos V, Zirkin BR, Hardy MP. In search of rat stem Leydig cells: identification, isolation, and lineage-specific development. Proc Natl Acad Sci USA 2006; 103: 2719-2724. DOI: 10.1073/pnas.0507692103

Hall AP. Review of the pericyte during angiogenesis and its role in cancer and diabetic retinopathy. Toxicol Pathol 2006; 34: 763-775. DOI: 10.1080/01926230600936290

Diaz-Flores L, Gutiérrez R, Garcia MP, Diaz-Flores L Jr, Valladares F, Madrid JF. Ultrastructure of myopericytoma: a continuum of transitional phenotypes of myopericytes. Ultrastr Pathol 2012; 36: 189-194. DOI: 10.3109/01913123.2012.655855

Ribatti D, Vacca A. Overview of angiogenesis during tumor growth. In: Figg WD, Folkman J (Eds), Angiogenesis. An Integrative Approach from Science to Medicine, Springer 2008; pp 161-167.

Hosaka K, Yang Y, Sekia T, Fischera C, Dubeya O, Fredlundc E, et al. Pericyte–fibroblast transition promotes tumor growth and metastasis. Proc Natl Acad Sci USA 2016; 113(36): E5618-E5627. DOI: 10.1073/pnas.1608384113

Rowley JE, Johnson JR. Pericytes in chronic lung disease. Int Arch Allergy Immunol 2014; 164:178–188. DOI: 10.1159/000365051

Basciani S , Mariani S , Arizzi M , Ulisse S, Rucci N ,Jannini EA, et al. 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 2002; 87: 2310–2319. DOI: 10.1210/jcem.87.5.8476

Gnessi L, Emidi A, Jannini EA, Carosa E, Maroder M, Arizzi M, et al. Testicular development involves the spatiotemporal control of PDGFs and PDGF receptors gene expression and action. J Cell Biol 1995; 131:1105-1121.

Gnessi L, Basciani S, Mariani S, Arizzi M, Spera G, Wang C, et al. Leydig cell loss and spermatogenic arrest in platelet-derived growth factor (PDGF)-A-deficient mice. J Cell Biol 2000; 149: 1019-1025.

Mariani S, Basciani S, Arizzi M, Spera G, Gnessi L. PDGF and the testis. Trends Endocrinol Metab 2002; 13: 11-17. DOI: 10.1016/S1043-2760(01)00518-5

Shan L-X, Zhu L-J, Bardin CW, Hardy MP. Quantitative analysis of androgen receptor messenger ribonucleic acid in developing Leydig cells and Sertolli cells by in situ hybridiszation. Endocrinology 1995; 136: 3856- 3862. DOI: 10.1210/endo.136.9.7649092

Welsh M, Saunders PT, Atanassova N, Sharpe R, Smith LB. Androgen action via testicular peritubular myoid cells is essential for male fertility. FASEB J 2009; 23: 4218–4230. DOI: 10.1096/fj.09-138347

Welsh M, Sharpe RM, Moffat L, Atanassova N, Saunders PTK, Kilter S, et al. Androgen action via testicular arteriole smooth muscle cells is important for Leydig cell function, vasomotion and testicular fluid dynamics. PLoS ONE 2010; 5(10): e13632. DOI:10.1371/journal.pone.0013632

Welsh M, Moffat L, Belling K, de França LR, Segatelli TM, Saunders PTK et al. Androgen receptor signaling in peritubular myoid cells is essential for normal differentiation and function of adult Leydig cells. Int J Androl 2011; 35: 25-40. DOI:10.1111/j.1365-2605.2011.01150.x

Bergh A, Amber JED. Immunohistochemical demonstration of androgen receptors on testicular blood vessels. Int J Androl 1992; 15: 425-434. DOI: 10.1111/j.1365-2605.1992.tb01357.x

Huang C-K, Tsai M-Y, Luo J, Kang H-Y, Lee SO, Chang C. Suppression of androgen receptor enhances the selfrenewal of mesenchymal stem cells through elevated expression of EGFR. Biochim Biophy Acta 2013; 1833: 1222-1234. DOI: 10.1016/j.bbamcr.2013.01.007

Shan L-X, Bardin CW, Hardy MP. Immunohistochemical analysis of androgen effects on androgen receptor expression in developing Leydig and Sertoli cells. Endocrinology 1997; 138: 1259-1266. DOI:10.1210/endo.138.3.4973

Takamoto N, You L-R, Moses K, Chiang C, Zimmer WE, Schwartz RJ, et al. COUP-TFII is essential for radial and anteroposterior pattering of the stomach. Development 2005; 132: 2179- 2189. DOI: 10.1242/dev.01808

Shibata H, Ikeda Y, Mukai T, Morohashi K-i, Kurihara I, Ando T, et al. Expression profiles of COUP-TF, DAX-1, and SF-1 in human adrenal gland and adrenocortical tumors: possible implications in steroidogenesis. Mol Gen Metab 2001; 74: 206-216. DOI: 10.1006/mgme.2001.3231

Bischofberger J, Schmidt-Hieber C. Adulte Neurogenese im Hippocampus. Neuroforum 2006; 3: 212-221.

Dardick I, Poznanski WJ, Waheed I, Setterfield G. Ultrastructural observations on differentiating human preadipocytes cultured in vitro. Tissue Cell 1976; 8: 561–571.

Rolandsson S, Sjöland AA, Brune JC, Li H, Kassem M, Mertens F, et al. Primary mesenchymal stem cells in human transplanted lungs are CD90/CD105 perivascularly located tissue-resident cells. BMJ Open Resp Res 2014; 1:e000027. DOI:10.1136/bmjresp-2014-000027

Yang J, Weinberg RA. Epithelial-mesenchymal transition: At the crossroads of development and tumor metastasis. Dev Cell 2008; 14: 818-829.

Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009; 119: 1420-1428.

Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 2014; 15: 178-196. DOI: 10.1038/nrm3758

Tavazoie M, Van der Veke L, Silva-VargaV, Louissaint M, Colonna L, Zaidi B, et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008; 3: 279–288. DOI: 10.1016/j.stem.2008.07.025

Yao HH-C, Barsoum I. 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, 2007; pp. 47-54.

Kennedy E, Mooney CJ, Hakimjavadi R, Fitzpatrick E, Guha S, Collins LE, et al. Adult vascular smooth muscle cells in culture express neural stem cell markers typical of resident multipotent vascular stem cells. Cell Tissue Res 2014; 358: 203-216. DOI 10.1007/s00441-014-1937-2




DOI: http://dx.doi.org/10.14748/bmr.v28.4448

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Michail S. Davidoff
University Medical Center Hamburg-Eppendorf, Hamburg
Germany

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