Comparative characterization of cells from the various compartments of the human umbilical cord shows that the Wharton's jelly compartment provides the best source of clinically utilizable mesenchymal stem cells

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Subramanian, Arjunan ^a   Fong, Chui Yee ^a   Biswas, Arijit ^a   Bongso, Ariff ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; BETA1 INTEGRIN; CD108 ANTIGEN; CD24 ANTIGEN; ENDOGLIN; HERMES ANTIGEN; HLA ANTIGEN; LYMPHOCYTE ANTIGEN; TELOMERASE; THY 1 ANTIGEN; UNCLASSIFIED DRUG;

ADIPOCYTE; AMNION CELL; ARTICLE; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYONIC STEM CELL; EPITHELIUM CELL; FLUORESCENCE ANALYSIS; HISTOLOGY; HUMAN; HUMAN CELL; KARYOTYPE; MESENCHYMAL STEM CELL; OSTEOCYTE; PERIVASCULAR CELL; PHENOTYPE; SUBAMNION CELL; UMBILICAL CORD; WHARTON JELLY; CELL CULTURE TECHNIQUE; CYTOLOGY; FEMALE; FIBROBLAST; MESENCHYMAL STROMA CELL; PHYSIOLOGY; PLURIPOTENT STEM CELL; PREGNANCY; PROCEDURES;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; FEMALE; FIBROBLASTS; HUMANS; MESENCHYMAL STROMAL CELLS; PLURIPOTENT STEM CELLS; PREGNANCY; UMBILICAL CORD;

EID: 84936763632     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127992     Document Type: Article

References (80)

1. Rao MS, Mattson MP. Stem cells and aging: expanding the possibilities. Mechanisms of ageing and development. 2001; 122(7):713-34. PMID: 11322994.
2. Baksh D, Yao R, Tuan RS. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem cells. 2007; 25(6):1384-92. doi: 10.1634/stemcells.2006-0709 PMID: 17332507.
3. Sarugaser R, Lickorish D, Baksh D, Hosseini MM, Davies JE. Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem cells. 2005; 23(2):220-9. doi: 10.1634/stemcells.2004-0166 PMID: 15671145.
4. Ilancheran S, Michalska A, Peh G, Wallace EM, Pera M, Manuelpillai U. Stem cells derived from human fetal membranes display multilineage differentiation potential. Biology of reproduction. 2007; 77(3):577-88. doi: 10.1095/biolreprod.106.055244 PMID: 17494917.
5. Troyer DL, Weiss ML. Concise review: Wharton's jelly-derived cells are a primitive stromal cell population. Stem cells. 2008; 26(3):591-9. Epub 2007/12/11. doi: 10.1634/stemcells.2007-0439 PMID: 18065397; PubMed Central PMCID: PMCPmc3311226.
6. Schugar RC, Chirieleison SM, Wescoe KE, Schmidt BT, Askew Y, Nance JJ, et al. High harvest yield, high expansion, and phenotype stability of CD146 mesenchymal stromal cells from whole primitive human umbilical cord tissue. Journal of biomedicine & biotechnology. 2009; 2009:789526. Epub 2009/12/29. doi: 10.1155/2009/789526 PMID: 20037738; PubMed Central PMCID: PMCPmc2796378.
7. Kita K, Gauglitz GG, Phan TT, Herndon DN, Jeschke MG. Isolation and characterization of mesenchymal stem cells from the sub-amniotic human umbilical cord lining membrane. Stem cells and development. 2010; 19(4):491-502. doi: 10.1089/scd.2009.0192 PMID: 19635009.
8. Conconi MT, Liddo RD, Tommasini M, Calore C, Parnigotto PP. Phenotype and Differentiation Potential of Stromal Populations Obtained from Various Zones of Human Umbilical Cord: An Overview. Open Tissue Engineering and Regenerative Medicine Journal. 2011; 4(SPEC. ISSUE 1):6-20.
9. Spurway J, Logan P, Pak S. The development structure and blood flow within the umbilical cord with particular reference to the venous system. Australasian Journal of Ultrasound in Medicine. 2012; 15(3):97-102.
10. Bongso A, Fong CY. The therapeutic potential, challenges and future clinical directions of stem cells from the Wharton's jelly of the human umbilical cord. Stem cell reviews. 2013; 9(2):226-40. doi: 10.1007/s12015-012-9418-z PMID: 23233233.
11. Weiss ML, Troyer DL. Stem cells in the umbilical cord. Stem cell reviews. 2006; 2(2):155-62. Epub 2007/01/24. doi: 10.1007/s12015-006-0022-y PMID: 17237554; PubMed Central PMCID: PMCPmc3753204.
12. Seshareddy K, Troyer D, Weiss ML. Method to isolate mesenchymal-like cells from Wharton's Jelly of umbilical cord. Methods in cell biology. 2008; 86:101-19. Epub 2008/04/30. doi: 10.1016/s0091-679x(08)00006-x PMID: 18442646.
13. Wang HS, Hung SC, Peng ST, Huang CC, Wei HM, Guo YJ, et al. Mesenchymal stem cells in the Wharton's jelly of the human umbilical cord. Stem cells. 2004; 22(7):1330-7. Epub 2004/12/08. doi: 10.1634/stemcells.2004-0013 PMID: 15579650.
14. Fong CY, Richards M, Manasi N, Biswas A, Bongso A. Comparative growth behaviour and characterization of stem cells from human Wharton's jelly. Reproductive biomedicine online. 2007; 15(6):708-18. PMID: 18062871.
15. Fong CY, Subramanian A, Biswas A, Gauthaman K, Srikanth P, Hande MP, et al. Derivation efficiency, cell proliferation, freeze-thaw survival, stem-cell properties and differentiation of human Wharton's jelly stem cells. Reproductive biomedicine online. 2010; 21(3):391-401. doi: 10.1016/j.rbmo.2010.04.010 PMID: 20638335.
16. Angelucci S, Marchisio M, Di Giuseppe F, Pierdomenico L, Sulpizio M, Eleuterio E, et al. Proteome analysis of human Wharton's jelly cells during in vitro expansion. Proteome science. 2010; 8:18. Epub 2010/03/30. doi: 10.1186/1477-5956-8-18 PMID: 20346146; PubMed Central PMCID: PMCPmc2867805.
17. Kikuchi-Taura A, Taguchi A, Kanda T, Inoue T, Kasahara Y, Hirose H, et al. Human umbilical cord provides a significant source of unexpanded mesenchymal stromal cells. Cytotherapy. 2012; 14(4):441-50. Epub 2012/02/22. doi: 10.3109/14653249.2012.658911 PMID: 22339605.
18. Bosch J, Houben AP, Radke TF, Stapelkamp D, Bunemann E, Balan P, et al. Distinct differentiation potential of "MSC" derived from cord blood and umbilical cord: are cord-derived cells true mesenchymal stromal cells? Stem cells and development. 2012; 21(11):1977-88. Epub 2011/11/18. doi: 10.1089/scd.2011.0414 PMID: 22087798.
19. Capelli C, Gotti E, Morigi M, Rota C, Weng L, Dazzi F, et al. Minimally manipulated whole human umbilical cord is a rich source of clinical-grade human mesenchymal stromal cells expanded in human platelet lysate. Cytotherapy. 2011; 13(7):786-801. doi: 10.3109/14653249.2011.563294 WOS:000293868300003. PMID: 21417678
20. Jeschke MG, Gauglitz GG, Phan TT, Herndon DN, Kita K. Umbilical cord lining membrane and wharton's jelly-derived mesenchymal stem cells: The similarities and differences. Open Tissue Engineering and Regenerative Medicine Journal. 2011; 4(SPEC. ISSUE 1):21-7.
21. Mihu CM, Rus Ciuca D, Soritau O, Susman S, Mihu D. Isolation and characterization of mesenchymal stem cells from the amniotic membrane. Romanian journal of morphology and embryology = Revue roumaine de morphologie et embryologie. 2009; 50(1):73-7. PMID: 19221648.
22. Diaz-Prado S, Muinos-Lopez E, Hermida-Gomez T, Rendal-Vazquez ME, Fuentes-Boquete I, de Toro FJ, et al. Isolation and Characterization of Mesenchymal Stem Cells from Human Amniotic Membrane. Tissue engineering Part C, Methods. 2010. doi: 10.1089/ten.TEC.2010.0136 PMID: 20673138.
23. Sarugaser R, Hanoun L, Keating A, Stanford WL, Davies JE. Human mesenchymal stem cells self-renew and differentiate according to a deterministic hierarchy. PloS one. 2009; 4(8):e6498. doi: 10.1371/journal.pone.0006498 PMID: 19652709; PubMed Central PMCID: PMC2714967.
24. Farias VA, Linares-Fernandez JL, Penalver JL, Paya Colmenero JA, Ferron GO, Duran EL, et al. Human umbilical cord stromal stem cell express CD10 and exert contractile properties. Placenta. 2011; 32(1):86-95. doi: 10.1016/j.placenta.2010.11.003 PMID: 21126763.
25. Martin-Rendon E, Sweeney D, Lu F, Girdlestone J, Navarrete C, Watt SM. 5-Azacytidine-treated human mesenchymal stem/progenitor cells derived from umbilical cord, cord blood and bone marrow do not generate cardiomyocytes in vitro at high frequencies. Vox sanguinis. 2008; 95(2):137-48. Epub 2008/06/19. doi: 10.1111/j.1423-0410.2008.01076.x PMID: 18557828.
26. Reza HM, Ng BY, Phan TT, Tan DT, Beuerman RW, Ang LP. Characterization of a novel umbilical cord lining cell with CD227 positivity and unique pattern of P63 expression and function. Stem cell reviews. 2011; 7(3):624-38. doi: 10.1007/s12015-010-9214-6 PMID: 21181306.
27. Gonzalez R, Griparic L, Umana M, Burgee K, Vargas V, Nasrallah R, et al. An efficient approach to isolation and characterization of pre- and postnatal umbilical cord lining stem cells for clinical applications. Cell transplantation. 2010; 19(11):1439-49. doi: 10.3727/096368910X514260 PMID: 20587136.
28. Jo CH, Kim OS, Park EY, Kim BJ, Lee JH, Kang SB, et al. Fetal mesenchymal stem cells derived from human umbilical cord sustain primitive characteristics during extensive expansion. Cell and tissue research. 2008; 334(3):423-33. Epub 2008/10/23. doi: 10.1007/s00441-008-0696-3 PMID: 18941782.
29. Secco M, Moreira YB, Zucconi E, Vieira NM, Jazedje T, Muotri AR, et al. Gene expression profile of mesenchymal stem cells from paired umbilical cord units: cord is different from blood. Stem cell reviews. 2009; 5(4):387-401. Epub 2010/01/09. doi: 10.1007/s12015-009-9098-5 PMID: 20058202; PubMed Central PMCID: PMCPmc2803263.
30. Nanaev AK, Kohnen G, Milovanov AP, Domogatsky SP, Kaufmann P. Stromal differentiation and architecture of the human umbilical cord. Placenta. 1997; 18(1):53-64. Epub 1997/01/01. PMID: 9032810.
31. Ishige I, Nagamura-Inoue T, Honda MJ, Harnprasopwat R, Kido M, Sugimoto M, et al. Comparison of mesenchymal stem cells derived from arterial, venous, and Wharton's jelly explants of human umbilical cord. International journal of hematology. 2009; 90(2):261-9. Epub 2009/08/07. doi: 10.1007/s12185-009-0377-3 PMID: 19657615.
32. La Rocca G, Anzalone R, Corrao S, Magno F, Loria T, Lo Iacono M, et al. Isolation and characterization of Oct-4+/HLA-G+ mesenchymal stem cells from human umbilical cord matrix: differentiation potential and detection of new markers. Histochemistry and cell biology. 2009; 131(2):267-82. doi: 10.1007/s00418-008-0519-3 PMID: 18836737.
33. Hass R, Kasper C, Bohm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell communication and signaling: CCS. 2011; 9:12. Epub 2011/05/17. doi: 10.1186/1478-811x-9-12 PMID: 21569606; PubMed Central PMCID: PMCPmc3117820.
34. Gauthaman K, Richards M, Wong J, Bongso A. Comparative evaluation of the effects of statins on human stem and cancer cells in vitro. Reproductive biomedicine online. 2007; 15(5):566-81. PMID: 18028750.
35. Mennan C, Wright K, Bhattacharjee A, Balain B, Richardson J, Roberts S. Isolation and characterisation of mesenchymal stem cells from different regions of the human umbilical cord. BioMed research international. 2013; 2013:916136. doi: 10.1155/2013/916136 PMID: 23984420; PubMed Central PMCID: PMC3741948.
36. Wetzig A, Alaiya A, Al-Alwan M, Pradez CB, Pulicat MS, Al-Mazrou A, et al. Differential marker expression by cultures rich in mesenchymal stem cells. BMC cell biology. 2013; 14:54. doi: 10.1186/1471-2121-14-54 PMID: 24304471; PubMed Central PMCID: PMC4235221.
37. Chatzigeorgiou A, Lyberi M, Chatzilymperis G, Nezos A, Kamper E. CD40/CD40L signaling and its implication in health and disease. BioFactors. 2009; 35(6):474-83. doi: 10.1002/biof.62 PMID: 19904719.
38. Somasundaram I, Mishra R, Radhakrishnan H, Sankaran R, Garikipati VN, Marappagounder D. Human adult stem cells maintain a constant phenotype profile irrespective of their origin, Basal media, and long term cultures. Stem cells international. 2015; 2015:146051. doi: 10.1155/2015/146051 PMID: 25688272; PubMed Central PMCID: PMC4320880.
39. Mafi P, Hindocha S, Mafi R, Griffin M, Khan WS. Adult mesenchymal stem cells and cell surface characterization - a systematic review of the literature. The open orthopaedics journal. 2011; 5(Suppl 2):253-60. doi: 10.2174/1874325001105010253 PMID: 21966340; PubMed Central PMCID: PMC3178966.
40. Zhang H, Zhang B, Tao Y, Cheng M, Hu J, Xu M, et al. Isolation and characterization of mesenchymal stem cells from whole human umbilical cord applying a single enzyme approach. Cell biochemistry and function. 2012; 30(8):643-9. doi: 10.1002/cbf.2843 PMID: 22777760.
41. Nagamura-Inoue T, He H. Umbilical cord-derived mesenchymal stem cells: Their advantages and potential clinical utility. World journal of stem cells. 2014; 6(2):195-202. Epub 2014/04/29. doi: 10.4252/wjsc.v6.i2.195 PMID: 24772246; PubMed Central PMCID: PMCPmc3999777.
42. Ben-David U, Benvenisty N. The tumorigenicity of human embryonic and induced pluripotent stem cells. Nature reviews Cancer. 2011; 11(4):268-77. Epub 2011/03/11. doi: 10.1038/nrc3034 PMID: 21390058.
43. Bara JJ, Richards RG, Alini M, Stoddart MJ. Concise review: Bone marrow-derived mesenchymal stem cells change phenotype following in vitro culture: implications for basic research and the clinic. Stem cells. 2014; 32(7):1713-23. Epub 2014/01/23. doi: 10.1002/stem.1649 PMID: 24449458.
44. Blasi A, Martino C, Balducci L, Saldarelli M, Soleti A, Navone SE, et al. Dermal fibroblasts display similar phenotypic and differentiation capacity to fat-derived mesenchymal stem cells, but differ in anti-inflammatory and angiogenic potential. Vascular cell. 2011; 3(1):5. doi: 10.1186/2045-824X-3-5 PMID: 21349162; PubMed Central PMCID: PMC3044104.
45. Weiss ML, Medicetty S, Bledsoe AR, Rachakatla RS, Choi M, Merchav S, et al. Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson's disease. Stem cells. 2006; 24(3):781-92. Epub 2005/10/15. doi: 10.1634/stemcells.2005-0330 PMID: 16223852.
46. Caplan AI. All MSCs are pericytes? Cell stem cell. 2008; 3(3):229-30. Epub 2008/09/13. doi: 10.1016/j.stem.2008.08.008 PMID: 18786406.
47. Covas DT, Panepucci RA, Fontes AM, Silva WA Jr., Orellana MD, Freitas MC, et al. Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Experimental hematology. 2008; 36(5):642-54. Epub 2008/02/26. doi: 10.1016/j.exphem.2007.12.015 PMID: 18295964.
48. Gauthaman K, Fong CY, Suganya CA, Subramanian A, Biswas A, Choolani M, et al. Extra-embryonic human Wharton's jelly stem cells do not induce tumorigenesis, unlike human embryonic stem cells. Reproductive biomedicine online. 2012; 24(2):235-46. doi: 10.1016/j.rbmo.2011.10.007 PMID: 22196893.
49. Gutierrez-Aranda I, Ramos-Mejia V, Bueno C, Munoz-Lopez M, Real PJ, Macia A, et al. Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless the site of injection. Stem cells. 2010; 28(9):1568-70. doi: 10.1002/stem.471 PMID: 20641038; PubMed Central PMCID: PMC2996086.
50. Arnheim N, Cortopassi G. Deleterious mitochondrial DNA mutations accumulate in aging human tissues. Mutation research. 1992; 275(3-6):157-67. Epub 1992/09/01. PMID: 1383758.
51. Ono T, Uehara Y, Saito Y, Ikehata H. Mutation theory of aging, assessed in transgenic mice and knockout mice. Mechanisms of ageing and development. 2002; 123(12):1543-52. Epub 2002/12/10. PMID: 12470892.
52. Pera MF. Stem cells: Low-risk reprogramming. Nature. 2009; 458(7239):715-6. Epub 2009/04/11. doi: 10.1038/458715a PMID: 19360075.
53. Yang H, Xie Z, Wei L, Yang H, Yang S, Zhu Z, et al. Human umbilical cord mesenchymal stem cell-derived neuron-like cells rescue memory deficits and reduce amyloid-beta deposition in an AbetaPP/PS1 transgenic mouse model. Stem cell research & therapy. 2013; 4(4):76. Epub 2013/07/06. doi: 10.1186/scrt227 PMID: 23826983; PubMed Central PMCID: PMCPmc3854736.
54. Dalous J, Larghero J, Baud O. Transplantation of umbilical cord-derived mesenchymal stem cells as a novel strategy to protect the central nervous system: technical aspects, preclinical studies, and clinical perspectives. Pediatric research. 2012; 71(4 Pt 2):482-90. Epub 2012/03/21. doi: 10.1038/pr.2011.67 PMID: 22430384.
55. Mitchell KE, Weiss ML, Mitchell BM, Martin P, Davis D, Morales L, et al. Matrix cells from Wharton's jelly form neurons and glia. Stem cells. 2003; 21(1):50-60. doi: 10.1634/stemcells.21-1-50 PMID: 12529551.
56. Pereira WC, Khushnooma I, Madkaikar M, Ghosh K. Reproducible methodology for the isolation of mesenchymal stem cells from human umbilical cord and its potential for cardiomyocyte generation. Journal of tissue engineering and regenerative medicine. 2008; 2(7):394-9. Epub 2008/07/11. doi: 10.1002/term.107 PMID: 18615777.
57. Yan Y, Xu W, Qian H, Si Y, Zhu W, Cao H, et al. Mesenchymal stem cells from human umbilical cords ameliorate mouse hepatic injury in vivo. Liver international: official journal of the International Association for the Study of the Liver. 2009; 29(3):356-65. Epub 2009/01/15. doi: 10.1111/j.1478-3231.2008.01855.x PMID: 19141029.
58. Yoon JH, Roh EY, Shin S, Jung NH, Song EY, Lee DS, et al. Introducing pulsed low-intensity ultrasound to culturing human umbilical cord-derived mesenchymal stem cells. Biotechnology letters. 2009; 31(3):329-35. Epub 2008/11/06. doi: 10.1007/s10529-008-9872-5 PMID: 18985278.
59. Qiao C, Xu W, Zhu W, Hu J, Qian H, Yin Q, et al. Human mesenchymal stem cells isolated from the umbilical cord. Cell biology international. 2008; 32(1):8-15. doi: 10.1016/j.cellbi.2007.08.002 PMID: 17904875.
60. Chen MY, Lie PC, Li ZL, Wei X. Endothelial differentiation of Wharton's jelly-derived mesenchymal stem cells in comparison with bone marrow-derived mesenchymal stem cells. Experimental hematology. 2009; 37(5):629-40. Epub 2009/04/21. doi: 10.1016/j.exphem.2009.02.003 PMID: 19375653.
61. Majore I, Moretti P, Stahl F, Hass R, Kasper C. Growth and differentiation properties of mesenchymal stromal cell populations derived from whole human umbilical cord. Stem cell reviews. 2011; 7(1):17-31. doi: 10.1007/s12015-010-9165-y PMID: 20596801.
62. Zhang YN, Lie PC, Wei X. Differentiation of mesenchymal stromal cells derived from umbilical cord Wharton's jelly into hepatocyte-like cells. Cytotherapy. 2009; 11(5):548-58. doi: 10.1080/14653240903051533 PMID: 19657806.
63. Chao KC, Chao KF, Fu YS, Liu SH. Islet-like clusters derived from mesenchymal stem cells in Wharton's Jelly of the human umbilical cord for transplantation to control type 1 diabetes. PloS one. 2008; 3(1):e1451. doi: 10.1371/journal.pone.0001451 PMID: 18197261; PubMed Central PMCID: PMC2180192.
64. Wu KH, Zhou B, Lu SH, Feng B, Yang SG, Du WT, et al. In vitro and in vivo differentiation of human umbilical cord derived stem cells into endothelial cells. Journal of cellular biochemistry. 2007; 100(3):608-16. doi: 10.1002/jcb.21078 PMID: 16960877.
65. Conconi MT, Burra P, Di Liddo R, Calore C, Turetta M, Bellini S, et al. CD105(+) cells from Wharton's jelly show in vitro and in vivo myogenic differentiative potential. International journal of molecular medicine. 2006; 18(6):1089-96. PMID: 17089012.
66. Weiss ML, Anderson C, Medicetty S, Seshareddy KB, Weiss RJ, VanderWerff I, et al. Immune properties of human umbilical cord Wharton's jelly-derived cells. Stem cells. 2008; 26(11):2865-74. doi: 10.1634/stemcells.2007-1028 PMID: 18703664.
67. Weiss ML, Mitchell KE, Hix JE, Medicetty S, El-Zarkouny SZ, Grieger D, et al. Transplantation of porcine umbilical cord matrix cells into the rat brain. Experimental neurology. 2003; 182(2):288-99. PMID: 12895440.
68. Medicetty S, Bledsoe AR, Fahrenholtz CB, Troyer D, Weiss ML. Transplantation of pig stem cells into rat brain: proliferation during the first 8 weeks. Experimental neurology. 2004; 190(1):32-41. doi: 10.1016/j.expneurol.2004.06.023 PMID: 15473978.
69. Ayuzawa R, Doi C, Rachakatla RS, Pyle MM, Maurya DK, Troyer D, et al. Naive human umbilical cord matrix derived stem cells significantly attenuate growth of human breast cancer cells in vitro and in vivo. Cancer letters. 2009; 280(1):31-7. Epub 2009/03/17. doi: 10.1016/j.canlet.2009.02.011 PMID: 19285791; PubMed Central PMCID: PMCPmc2914472.
70. Ganta C, Chiyo D, Ayuzawa R, Rachakatla R, Pyle M, Andrews G, et al. Rat umbilical cord stem cells completely abolish rat mammary carcinomas with no evidence of metastasis or recurrence 100 days post-tumor cell inoculation. Cancer research. 2009; 69(5):1815-20. Epub 2009/02/27. doi: 10.1158/0008-5472.can-08-2750 PMID: 19244122.
71. Matsuzuka T, Rachakatla RS, Doi C, Maurya DK, Ohta N, Kawabata A, et al. Human umbilical cord matrix-derived stem cells expressing interferon-beta gene significantly attenuate bronchioloalveolar carcinoma xenografts in SCID mice. Lung cancer. 2010; 70(1):28-36. doi: 10.1016/j.lungcan.2010.01.003 PMID: 20138387; PubMed Central PMCID: PMC2930041.
72. Maurya DK, Doi C, Kawabata A, Pyle MM, King C, Wu Z, et al. Therapy with un-engineered naive rat umbilical cord matrix stem cells markedly inhibits growth of murine lung adenocarcinoma. BMC cancer. 2010; 10:590. doi: 10.1186/1471-2407-10-590 PMID: 21029413; PubMed Central PMCID: PMC2988749.
73. Ma Y, Hao X, Zhang S, Zhang J. The in vitro and in vivo effects of human umbilical cord mesenchymal stem cells on the growth of breast cancer cells. Breast cancer research and treatment. 2012; 133(2):473-85. doi: 10.1007/s10549-011-1774-x PMID: 21947651.
74. Chao KC, Yang HT, Chen MW. Human umbilical cord mesenchymal stem cells suppress breast cancer tumourigenesis through direct cell-cell contact and internalization. Journal of cellular and molecular medicine. 2012; 16(8):1803-15. doi: 10.1111/j.1582-4934.2011.01459.x PMID: 21973190.
75. Gauthaman K, Yee FC, Cheyyatraivendran S, Biswas A, Choolani M, Bongso A. Human umbilical cord Wharton's jelly stem cell (hWJSC) extracts inhibit cancer cell growth in vitro. Journal of cellular biochemistry. 2012; 113(6):2027-39. doi: 10.1002/jcb.24073 PMID: 22275115.
76. Gauthaman K, Fong CY, Arularasu S, Subramanian A, Biswas A, Choolani M, et al. Human Wharton's jelly stem cell conditioned medium and cell-free lysate inhibit human osteosarcoma and mammary carcinoma cell growth in vitro and in xenograft mice. Journal of cellular biochemistry. 2013; 114(2):366-77. doi: 10.1002/jcb.24367 PMID: 22930595.
77. Liu J, Han G, Liu H, Qin C. Suppression of cholangiocarcinoma cell growth by human umbilical cord mesenchymal stem cells: a possible role of Wnt and Akt signaling. PloS one. 2013; 8(4):e62844. doi: 10.1371/journal.pone.0062844 PMID: 23646150; PubMed Central PMCID: PMC3639969.
78. Wu S, Ju GQ, Du T, Zhu YJ, Liu GH. Microvesicles derived from human umbilical cord Wharton's jelly mesenchymal stem cells attenuate bladder tumor cell growth in vitro and in vivo. PloS one. 2013; 8(4): e61366. doi: 10.1371/journal.pone.0061366 PMID: 23593475; PubMed Central PMCID: PMC3625149.
79. Wang XY, Lan Y, He WY, Zhang L, Yao HY, Hou CM, et al. Identification of mesenchymal stem cells in aorta-gonad-mesonephros and yolk sac of human embryos. Blood. 2008; 111(4):2436-43. doi: 10.1182/blood-2007-07-099333 PMID: 18045971.
80. Yang HT, Chao KC. Foetal defence against cancer: a hypothesis. Journal of cellular and molecular medicine. 2013; 17(9):1096-8. doi: 10.1111/jcmm.12095 PMID: 23815673; PubMed Central PMCID: PMC4118168.