Umbilical cord revisited: From Wharton's jelly myofibroblasts to mesenchymal stem cells

Histology and Histopathology

Volumn 28, Issue 10, 2013, Pages 1235-1244

  Corrao, Simona ^a,b   La Rocca, Giampiero ^a,b   Lo Iacono, Melania ^a,b   Corsello, Tiziana ^a,b   Farina, Felicia ^a   Anzalone, Rita ^a  

^a UNIVERSITY OF PALERMO   (Italy)

^b Euro Mediterranean Institute of Science and Technology   (Italy)

Author keywords

Extracellular matrix; Immunomodulatory markers; Mesenchymal stem cells; Stromal myofibroblasts; Umbilical cord; Wharton's jelly

Indexed keywords

ANIMAL; BONE MARROW CELL; CELL DIFFERENTIATION; CYTOLOGY; EXTRACELLULAR MATRIX; FEMALE; HUMAN; MESENCHYMAL STROMA CELL; METABOLISM; MYOFIBROBLAST; PHENOTYPE; PHYSIOLOGY; PLACENTA; PREGNANCY; REGENERATIVE MEDICINE; REVIEW; STEM CELL; UMBILICAL CORD; WHARTON JELLY;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; EXTRACELLULAR MATRIX; FEMALE; HUMANS; MESENCHYMAL STROMAL CELLS; MYOFIBROBLASTS; PHENOTYPE; PLACENTA; PREGNANCY; REGENERATIVE MEDICINE; STEM CELLS; UMBILICAL CORD; WHARTON JELLY;

EID: 84885366206     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (102)

1. Alaminos M., Pérez-Köhler B., Garzón I., García-Honduvilla N., Romero B., Campos A. and Buján J. (2010). Transdifferentiation potentiality of human Wharton's jelly stem cells towards vascular endothelial cells. J. Cell. Physiol. 223, 640-647.
2. Anzalone R., La Rocca G., Di Stefano A., Magno F., Corrao S., Carbone M., Loria T., Lo Iacono M., Eleuteri E., Colombo M., Cappello F., Farina F., Zummo G. and Giannuzzi P. (2009). Role of endothelial cell stress in the pathogenesis of chronic heart failure. Front. Biosci. 14, 2238-2247.
3. Anzalone R., Lo Iacono M., Corrao S., Magno F., Loria T., Cappello F., Zummo G., Farina F. and La Rocca G. (2010). New emerging potentials for human Wharton's jelly mesenchymal stem cells: immunological features and hepatocyte-like differentiative capacity. Stem Cell Dev. 19, 423-438.
4. Anzalone R., Farina F., Zummo G. and La Rocca G. (2011a). Recent patents and advances on isolation and cellular therapy applications of mesenchymal stem cells from human umbilical cord Wharton's jelly. Recent Pat. Regen. Med. 1, 216-227.
5. Anzalone R., Lo Iacono M., Loria T., Di Stefano A., Giannuzzi P., Farina F. and La Rocca G. (2011b). Wharton's jelly mesenchymal stem cells as candidates for beta cells regeneration: extending the differentiative and immunomodulatory benefits of adult mesenchymal stem cells for the treatment of type 1 diabetes. Stem Cell Rev. 7, 342-363.
6. Anzalone R., Corrao S., Lo Iacono M., Loria T., Corsello T., Cappello F., Di Stefano A., Giannuzzi P., Zummo G., Farina F. and La Rocca G. (2013). Isolation and characterization of CD276+/HLA-E+ human subendocardial mesenchymal stem cells from chronic heart failure patients: analysis of differentiative potential and immunomodulatory markers expression. Stem Cells Dev. 22, 1-17.
7. Ayuzawa R., Doi C., Rachakatla R.S., Pyle M.M., Maurya D.K., Troyer D. and Tamura M. (2009). Naïve human umbilical cord matrix derived stem cells significantly attenuate growth of human breast cancer cells in vitro and in vivo. Cancer Lett. 280, 31-37.
8. Bańkowski E., Sobolewski K., Romanowicz L., Chyczewski L. and Jaworski S. (1996). Collagen and glycosaminoglycans of Wharton's jelly and their alterations in EPH-gestosis. Eur. J. Obstet. Gynecol. 66, 109-117.
9. Bańkowski E., Pawlicka E. and Jaworski S. (2000). Stimulation of collagen biosynthesis by the umbilical cord serum of newborns delivered by mothers with EPH-gestosis (preeclampsia). Clin. Chim. Acta. 302, 23-34.
10. Campard D., Lysy P.A., Najimi M. and Sokal E.M. (2008). Native umbilical cord matrix stem cells express hepatic markers and differentiate into hepatocyte-like cells. Gastroenterology 134, 833-848.
11. Can A. and Karahuseyinoglu S. (2007). Concise review: human umbilical cord stroma with regard to the source of fetus-derived stem cells. Stem Cells 25, 2886-2895.
12. Cappello F., Di Stefano A., David S., Rappa F., Anzalone R., La Rocca G., D'Anna S.E., Magno F., Donner C.F., Balbi B. and Zummo G. (2006). Hsp60 and Hsp10 down-regulation predicts bronchial epithelial carcinogenesis in smokers with chronic obstructive pulmonary disease. Cancer 107, 2417-2424.
13. Cappello F., Czarnecka A.M., La Rocca G., Di Stefano A., Zummo G. and Macario A.J. (2007). Hsp60 and Hsp10 as antitumor molecular agents. Cancer Biol. Ther. 6, 487-489.
14. Charausia B.D. and Agarwal B.M. (1979). Helical structure of the human umbilical cord. Acta Anat. (Basel). 103, 226-230.
15. Conconi M.T., Di Liddo R., Tommasini M., Calore C. and Parnigotto P.P. (2011). Phenotype and differentiation potential of stromal populations obtained from various zones of human umbilical cord: an overview. Open Tissue Eng. Regen. Med. J. 4, 6-20.
16. Copland I.B., Adamson S.L., Post M., Lye S.J. and Caniggia I. (2002). TGF-ß3 expression during umbilical cord development and its alteration in pre-eclampsia. Placenta. 23, 311-321.
17. Corrao S., Campanella C., Anzalone R., Farina F., Zummo G., Conway de Macario E., Macario A.J.L., Cappello F. and La Rocca G. (2010). Human Hsp10 and Early Pregnancy Factor (EPF) and their relationship and involvement in cancer and immunity: Current knowledge and perspectives. Life Sci. 86, 145-152.
18. Corrao S., La Rocca G., Lo Iacono M., Zummo G., Gerbino A., Farina F. and Anzalone R. (2013). New Frontiers in Regenerative Medicine in Cardiology: The Potential of Wharton's Jelly Mesenchymal Stem Cells. Curr. Stem Cell Res. Ther. 8, 39-45.
19. Davis J.P.L., Chien P.F.-W, Chipperfield A.R., Gordon A. and Harper A.A. (2000). The three mechanisms of intracellular chloride accumulation in vascular smooth muscle of human umbilical and placental arteries. Pflügers Arch.-Eur. J. Physiol. 441, 150-154.
20. De Kock J., Najar M., Bolleyn J., Al Battah F., Rodrigues R.M., Buyl K., Raicevic G., Govaere O., Branson S., Meganathan K., Gaspar J.A., Roskams T., Sachinidis A., Lagneaux L., Vanhaecke T. and Rogiers V. (2012). Mesoderm-derived stem cells: the link between the transcriptome and their differentiation potential. Stem Cells Dev. 21, 3309-3323.
21. Di Naro E., Ghezzi F., Raio L., Franchi M. and D'Addario V. (2001). Umbilical cord morphology and pregnancy outcome. Eur. J. Obstet. Gynecol. Reprod. Biol. 96, 150-157.
22. Eleuteri E., Di Stefano A., Ricciardolo F.L., Magno F., Gnemmi I., Colombo M., Anzalone R., Cappello F., La Rocca G., Tarro Genta F., Zummo G. and Giannuzzi P. (2009). Increased nitrotyrosine plasma levels in relation to systemic markers of inflammation and myeloperoxidase in chronic heart failure. Int. J. Cardiol. 135, 386-390.
23. Eyden B.P., Ponting J., Davies H., Bartley C. and Torgersen E. (1994). Defining the myofibroblast: Normal tissues, with special reference to the stromal cells of Wharton's jelly in human umbilical cord. J. Submicrosc. Cytol. Pathol. 26, 347-355.
24. Felton C.V., Chang T.C., Crook D., Marsh M., Robson S.C. and Spencer J.A.D. (1994). Umibilical vessel wall fatty acids after normal and retarded fetal growth. Arch. Dis. Child. Fet. Neonatal. Ed. 70, F36-F39.
25. Ferguson V.L. and Dodson R.B. (2009). Bioengineering aspects of the umbilical cord. Eur. J. Obstet. Gynecol. Reprod. Biol. 144 (1), S108-S113.
26. Franc S., Rousseau J.C., Garrone R., van der Rest M. and Moradi- Améli M. (1998). Microfibrillar composition of umbilical cord matrix: characterization of fibrillin, collagen VI and intact collagen V. Placenta 19, 95-104.
27. Gabbiani G., Hirschel B.J., Ryan G.B., Statkov P.R. and Majno G. (1972). Granulation tissue as a contractile organ. J. Exp. Med. 135, 719-734.
28. Galewska Z., Romanowicz L., Jaworski S. and Bańkowski E. (2008). Gelatinase matrix metalloproteinase (MMP)-2 and MMP-9 of the umbilical cord blood in preeclampsia. Clin. Chem. Lab. Med. 46, 517-522.
29. Ghezzi F., Raio L., Di Naro E., Franchi M., Buttarelli M. and Schneider H. (2002). First-trimester umbilical cord diameter: a novel marker of fetal aneuploidy. Ultrasound Obstet. Gynecol. 19, 235-239.
30. Ghosh K.G., Ghosh S.N. and Gupta A.B. (1984). Tensile properties of human umbilical cord. Indian J. Med. Res. 79, 538-541.
31. Gogiel T., Bańkowski E. and Jaworski S. (2003). Proteoglycans in Wharton's jelly. Int. J. Biochem. Cell Biol. 35, 1461-1469.
32. Gottfried E., Kunz-Schughart L.A., Weber A., Rehli M., Peuker A., Müller A., Kastenberger M., Brockhoff G., Andreesen R. and Kreutz M. (2008). Expression of CD68 in non-myeloid cell types. Scand. J. Immunol. 67, 453-463.
33. Hass R., Kasper C., Böhm S. and Jacobs R. (2011). Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Commun. Signal. 14, 9-12.
34. Hollweck T., Hartmann I., Eblenkamp M., Wintermantle E., Reichart B., Überfuhr P. and Eissner G. (2011). Cardiac differentiation of human Wharton's jelly stem cells-experimental comparison of protocols. Open Tissue Eng. Regen. Med. J. 4, 95-102.
35. Hoyes A.D. (1968a). Ultrastructure of the cells of the amniotic fluid. J. Obstet. Gynaec. Br. Commonw. 75, 164-171.
36. Hoyes A.D. (1968b). Electron microscopy of the surface layer (periderm) of human foetal skin. J. Anat. 103, 321-336.
37. Hoyes A.D. (1969). Ultrastructure of the epithelium of the human umbilical cord. J. Anat. 150, 149-162.
38. Huang Y.C., Parolini O., La Rocca G. and Deng L. (2012). Umbilical cord versus bone marrow derived mesenchymal stromal cells. Stem Cells Dev. 21, 2900-2903.
39. Ichinose M, Takemura T, Andoh K, Sugimoto M. (2010). Pathological analysis of umbilical cord ulceration associated with fetal duodenal and jejunal atresia. Placenta 31, 1015-1018.
40. Jeschke M.G., Gauglitz G.G., Phan T.T., Herndon D.N., and Kita K. (2011). Umbilical cord lining membrane and Wharton's jelly-derived mesenchymal stem cells: the similarities and differences. Open Tissue Eng. Regen. Med. J. 4, 21-27.
41. Karahuseyinoglu S., Cinar O., Kilic E., Kara F., Akay G.G., Demiralp D.O., Tukun A., Uckan D. and Can A. (2007). Biology of stem cells in human umbilical cord stroma: in situ and in vitro surveys. Stem Cell 25, 319-331.
42. Kim K.S., Kim Y.S., Lim J.I., Jung M.H. and Park H.K. (2012). Nanoscale imaging of morphological changes of umbilical cord in pre-eclampsia. Microsc. Res. Tech. 75, 1445-1451.
43. Kita K., Gauglitz G.G., Phan T.T., Herdon D.N. and Jeschke M.G. (2010). Isolation and characterization of mesenchymal stem cells from the sub-amniotic human umbilical cord lining membrane. Stem Cell Dev. 19, 491-502.
44. Kobayashi K., Kubota T. and Aso T. (1998). Study on myofibroblast differentiation in the stromal cells of Wharton's jelly: Expression and localization of alpha-smooth muscle actin. Early Hum. Dev. 51, 223-233.
45. Kocaefe C., Balci D., Hayta B.B. and Can A. (2010). Reprogramming of human umbilical cord stromal mesenchymal stem cells for myogenic differentiation and muscle repair. Stem Cell Rev. 6, 512-522.
46. La Rocca G. (2011). Connecting the dots: The promises of Wharton's jelly mesenchymal stem cells for tissue repair and regeneration. Open Tissue Eng. Regen. Med. J. 4, 3-5.
47. La Rocca G. and Anzalone R. (2013). Perinatal stem cells revisited: directions and indications at the crossroads between tissue regeneration and repair. Curr. Stem Cell Res. Ther. 8, 2-5.
48. La Rocca G., Pucci-Minafra I., Marrazzo A., Taormina P. and Minafra S. (2004). Zymographic detection and clinical correlations of MMP-2 and MMP-9 in breast cancer sera. Br. J. Cancer 90, 1414-1421.
49. La Rocca G., Anzalone R., Magno F., Farina F., Cappello F. and Zummo G. (2007). Cigarette smoke exposure inhibits extracellular MMP-2 (gelatinase A) activity in human lung fibroblasts. Resp. Res. 8, 23.
50. La Rocca G., Di Stefano A., Eleuteri E., Anzalone R., Magno F., Corrao S., Loria T., Martorana A., Di Gangi C., Colombo M., Sansone F., Patanè F., Farina F., Rinaldi M., Cappello F., Giannuzzi P. and Zummo G. (2009a). Oxidative stress induces myeloperoxidase expression in endocardial endothelial cells from patients with chronic heart failure. Basic Res. Card. 104, 307-320.
51. La Rocca G., Anzalone R., Corrao S., Magno F., Loria T., Lo Iacono M., Di Stefano A., Giannuzzi P., Marasà L., Cappello F., Zummo G. and Farina F. (2009b). Isolation and characterization of Oct-4+/HLA-G+ mesenchymal stem cells from human umbilical cord matrix: differentiation potential and detection of new markers. Histochem. Cell Biol. 131, 267-282.
52. La Rocca G., Anzalone R. and Farina F. (2009c). The expression of CD68 in human umbilical cord mesenchymal stem cells: new evidences of presence in non-myeloid cell types. Scand. J. Immunol. 70, 161-162.
53. La Rocca G., Corrao S., Lo Iacono M., Corsello T., Farina F. and Anzalone R. (2012). Novel immunomodulatory markers expressed by human WJ-MSC: an updated review in regenerative and reparative medicine. Open Tissue Eng. Regen. Med. J. 5, 50-58.
54. La Rocca G., Lo Iacono M., Corsello T., Corrao S., Farina F. and Anzalone R. (2013). Human Wharton's jelly mesenchymal stem cells maintain the expression of key immunomodulatory molecules when subjected to osteogenic, adipogenic and chondrogenic differentiation in vitro: new perspectives for cellular therapy. Curr. Stem Cell Res. Ther. 8, 100-113.
55. Lo Iacono M., Anzalone R., Corrao S., Giuffrè M., Di Stefano A., Giannuzzi P., Cappello F., Farina F. and La Rocca G. (2011a). Perinatal and Wharton's jelly-derived mesenchymal stem cells in cartilage regenerative medicine and tissue engineering strategies. Open Tissue Eng. Regen. Med. J. 4, 72-81.
56. Lo Iacono M., Anzalone R., Corrao S., Zummo G., Farina F. and La Rocca G. (2011b). Non-classical type I HLAs and B7 costimulators revisited: analysis of expression and immunomodulatory role in undifferentiated and differentiated MSC isolated from human umbilical cord Wharton's jelly. Histol. Histopathol. 26 (1), 313.
57. Loeser R.F., Shanker G., Carlson C.S., Gardin J.F., Shelton B.J. and Sonntag W.E. (2000). Reduction in the chondrocyte response to insulinlike growth factor 1 in aging and osteoarthritis: studies in a non-human primate model of naturally occurring disease. Arthritis Rheum. 43, 2110-2120.
58. Majno, G., Gabbiani G., Hirschel B.J., Ryan G.B. and Statkov P.R. (1971). Contraction of granulation tissue in vitro: similarity to smooth muscle. Science (Washington). 173, 548-550.
59. Malcom J.E. and Pound D.P.B. (1971). Direction of spiral of the umbilical cord. J. R. Coll. Gen. Pract. 21, 746-747.
60. Malpas P. (1964). Length of the human umbilical cord at term. Br. Med. J. 1, 673-674.
61. Malpas P. and Symonds E.M. (1966). Observations on the structure of the human umbilical cord. Surg. Gynecol. Obstet. 123, 746-750.
62. Margossian T., Reppel L., Makdissy N., Stoltz J.F., Bensoussan D. and Huselstein C. (2012). Mesenchymal stem cells derived from Wharton's jelly: Comparative phenotype analysis between tissue and in vitro expansion. Biomed. Mater. Eng. 22, 243-254.
63. Martin B.F. and Tudor R.G. (1980). The umbilical and paraumbilical veins of man. J. Anat. 130, 305-322.
64. Martin J.A., Ellerbroek S.M. and Buckwalter J.A. (1997). Age-related decline in chondrocyte response to insulin-like growth factor-I: the role of growth factor binding proteins. J. Orthop. Res. 15, 491-498.
65. Mauro A., Buscemi M. and Gerbino A. (2010). Immunohistochemical and transcriptional expression of matrix metalloproteinases in full-term human umbilical cord and human umbilical vein endothelial cells. J. Mol. Histol. 41, 367-377.
66. Mauro A., Buscemi M., Provenzano S. and Gerbino A. (2011). Human umbilical cord expresses several vasoactive peptides involved in the local regulation of vascular tone: protein and gene expression of Orphanin, Oxytocin, ANP, eNOS and iNOS. Folia Histochem. Cytobiol. 49, 211-218.
67. McGuirk J.P. and Weiss M.L. (2011). Promising cellular therapeutics for prevention or management of graft-versus-host disease (a review). Placenta 32 (4), S304-S310.
68. Meyer F.A., Laver-Rudich Z. and Tanenbaum R. (1983). Evidence for a mechanical coupling of glycoprotein microfibrils with collagen fibrils in Wharton's jelly. Biochim. Biophys. Acta 755, 376-387.
69. Messai H., Duchossoy Y., Khatib A.M., Panasyuk A. and Mitrovic D. (2000). Articular chondrocytes from aging rats respond poorly to insulinlike growth factor-1: an altered signaling pathway. Mech. Ageing Dev. 115, 21-37.
70. Miki T., Lehmann T., Cai H., Stolz D.B. and Strom S.C. (2005). Stem cell characteristics of amniotic epithelial cells. Stem Cells 23, 1549-1559.
71. Mitchell K.E., Weiss M.L., Mitchell B.M., Martin P., Davis D., Morales L., Helwig B., Beerenstrauch M., Abou-Easa K., Hildreth T., Troyer D. and Medicetty S. (2003). Matrix cells from Wharton's jelly form neurons and glia. Stem Cells 21, 50-60.
72. Mizoguchi M., Suga Y., Sanmano B., Ikeda S. and Ogawa H. (2004). Organotypic culture and surface plantation using umbilical cord epithelial cells: morphogenesis and expression of differentiation markers mimicking cutaneous epidermis. J. Dermatol. Sci. 35, 199-206.
73. Myatt L. (1992). Control of vascular resistance in the human placenta. Placenta 13, 329-341.
74. Nanaev A.K., Kohen G., Milovanov A.P., Domogatsky S.P. and Kaufmann P. (1997). Stromal differentiation and architecture of the human umbilical cord. Placenta 18, 53-64.
75. Nekanti U., Rao V.B., Bahirvani A.G., Jan M., Totey S, Ta M. (2010). Long-term expansion and pluripotent marker array analysis of Wharton's jelly-derived mesenchymal stem cells. Stem Cells Dev. 19, 117-130.
76. Pałka J., Bańkowski E. and Jaworski S. (2000). An accumulation of IGF- I and IGF-binding proteins in human umbilical cord. Mol. Cell. Biochem. 206, 133-139.
77. Parry E.W. (1970). Some electron microscope observations on the mesenchymal structures of full-term umbilical cord. J. Anat. 107, 505-518.
78. Prasanna S.J. and Jahnavi V.S. (2011). Wharton's jelly mesenchymal stem cells as off-the-shelf cellular therapeutics: a closer look into their regenerative and immunomodulatory properties. Open Tissue Eng. Regen. Med. J. 4, 28-38.
79. Quan A., Leung S.W.S., Lao T.T., Man R.Y.K. (2003). 5- hydroxytryptamine and thromboxane A2 as physiologic mediators of human umbilical artery closure. J. Soc. Gynecol. Invest. 10, 490-495.
80. Rao C.V., Li X., Toth P. and Lei Z.M. (1995). Expression of epidermal growth factor, transforming growth factor-alpha, and their common receptor genes in human umbilical cords. J. Clin. Endocrinol. Metab. 80, 1012-1020.
81. Ryynänen J., Tan E.M., Hoffren J., Woodley D.T. and Sollberg S. (1993). Type VII collagen gene expression in human umbilical tissue and cells. Lab. Invest. 69, 300-304.
82. Romanov Y.A., Svintsitskaya V.A. and Smirnov V.N. (2003). Searching for alternative sources of postnatal human mesenchymal stem cells: candidate MSC-like cells from umbilical cord. Stem Cells 21, 105-110.
83. Romanowicz L. and Galewska Z. (2011).Extracellular matrix remodeling of the umbilical cord in pre-eclampsia as a risk factor for fetal hypertension. J. Pregnancy 2011, 542695
84. Sarugaser R., Lickorish D., Baksh D., Hosseini M.M. and Davies J. E. (2005). Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 23, 220-229.
85. Sarugaser R., Ennis J., Stanford W.L. and Davies J.E. (2009). Isolation, propagation, and characterization of human umbilical cord perivascular cells (HUCPVCs). Methods Mol. Biol. 482, 269-279.
86. Scott J.M. and Wilkinson R. (1978). Further studies on the umbilical cord and its water content. J. Clin. Pathol. 31, 944-948.
87. Sivalingam J., Krishnan S., Ng W.H., Lee S.S., Phan T.T. and Kon O.L. (2010). Biosafety assessment of site-directed transgene integration in human umbilical cord-lining cells. Mol. Ther. 18, 1346-1356.
88. Sobolewski K., Bańkowski E., Chyczewski L. and Jaworski S. (1997). Collagen and glycosaminoglycans of Wharton's jelly. Biol. Neonate 71, 11-21.
89. Sobolewski K., Małkowski A., Bańkowski E. and Jaworski S. (2005). Wharton's jelly as a reservoir of peptide growth factors. Placenta 26, 747-752.
90. Skulstad S.M., Ulriksen M., Rasmussen S. and Kiserud T. (2006). Effect of umbilical ring constriction on Wharton's jelly. Ultrasound Obstet. Gynecol. 28, 692-698.
91. Takechi K., Kuwabara Y. and Mizuno M. (1993). Ultrastructural and immunohistochemical studies of Wharton's jelly umbilical cord cells. Placenta 14, 235-245.
92. Tamura M., Kawabata A., Ohta N., Uppalapati L., Becker K.G. and Troyer D. (2011). Wharton's jelly stem cells as agents for cancer therapy Open Tissue Eng. Regen. Med. J. 4, 39-47.
93. Tantbirojn P., Saleemuddin A., Sirois K., Crum C.P., Boyd T.K., Tworoger S. and Parast M.M. (2009). Gross abnormalities of the umbilical cord: related placental histology and clinical significance. Placenta 30, 1083-1088.
94. Tee J.Y., Vaghjiani V., Liu Y.H., Murthi P., Chan J., Manuelpillai U. (2013). Immunogenicity and Immunomodulatory Properties of Hepatocyte-like Cells Derived from Human Amniotic Epithelial Cells. Curr. Stem Cell Res. Ther. 8, 91-99.
95. Troyer D.L. and Weiss M.L. (2008). Concise review: Wharton's jelly-derived cells are a primitive stromal cell population. Stem Cells 26, 591-599.
96. Vizza E., Correr S., Goranova V., Heyn R., Muglia U. and Papagianni V. (1995). The collagen fibrils arrangement in the Wharton's jelly of full-term human umbilical cord. Ital. J. Anat. Embryol. 100 (1), 495-501.
97. Vizza E., Correr S., Goranova V., Heyn R., Angelucci P.A., Forleo R. and Motta P.M. (1996). The collagen skeleton of the human umbilical cord at term. A scanning electron microscopy study after 2N-NaOH maceration. Reprod. Fertil. Dev. 8, 885-894.
98. Wang L., Tran I., Seshareddy K., Weiss M.L. and Detamore M.S. (2009). A comparison of human bone marrow-derived mesenchymal stem cells and human umbilical cord-derived mesenchymal stromal cells for cartilage tissue engineering. Tissue Eng. Part A 15, 2259-2266.
99. Wang L., Ott L., Seshareddy K., Weiss M.L. and Detamore MS. (2011). Musculoskeletal tissue engineering with human umbilical cord mesenchymal stromal cells. Regen. Med. 6, 95-109.
100. Weiss M.L., Anderson C., Medicetty S., Seshareddy K.B., Weiss R.J., Van der Werff I., Troyer D. and McIntosh K.R. (2008). Immune properties of human umbilical cord Wharton's jelly-derived cells. Stem Cells 26, 2865-2874.
101. Wyburn G.M. (1939). The formation of the umbilical cord and the umbilical region of the anterior abdominal wall. J. Anat. 73, 289-310.9.
102. Yamada K., Shimizu S. and Takahashi N. (1983). Histochemical demonstration of asparagine-linked oligosaccharides in glycoproteins of human placenta and umbilical cord tissues by means of almond glycopeptidase digestion. Histochem. J. 15, 1239-1250.