Positional identity of murine mesenchymal stem cells resident in different organs is determined in the postsegmentation mesoderm

Stem Cells and Development

Volumn 21, Issue 5, 2012, Pages 814-828

  Sági, Bernadett ^a   Maraghechi, Pouneh ^b   Urbán, Veronika S ^a,c   Hegyi, Beáta ^a   Szigeti, Anna ^a   Fajka Boja, Roberta ^d   Kudlik, Gyöngyi ^a   Német, Katalin ^a   Monostori, Éiva ^d   Gócza, Elen ^b   Uher, Ferenc ^a  

^a National Blood Service   (Hungary)

^b SZENT ISTVÁN UNIVERSITY   (Hungary)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ALPHA5 INTEGRIN; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; BRAIN DERIVED NEUROTROPHIC FACTOR; CD146 ANTIGEN; COLLAGEN TYPE 1; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 2; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH DIFFERENTIATION FACTOR 6; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; OSTEOCALCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SOMATOMEDIN C; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR PITX2; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR TBX5; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; VASCULOTROPIN A; VIMENTIN;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; AORTA; ARTICLE; BONE MARROW; CELL CULTURE; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; GENE IDENTIFICATION; HOX GENE; IN VITRO STUDY; MESENCHYMAL STEM CELL; MESODERM; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN; T LYMPHOCYTE; THYMUS;

ADIPOSE TISSUE; ANIMALS; AORTA; BLOTTING, WESTERN; BONE MARROW CELLS; CELL LINEAGE; CELLS, CULTURED; CLUSTER ANALYSIS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MESENCHYMAL STEM CELLS; MESODERM; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PAIRED BOX TRANSCRIPTION FACTORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN; T-BOX DOMAIN PROTEINS; THYMUS GLAND; TIME FACTORS;

MURINAE;

EID: 84859447666     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2011.0551     Document Type: Article

References (76)

1. Kolf CM, E Cho and RS Tuan. (2007). Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Res Ther 9:204
2. Chamberlain G, J Fox, B Ashton and J Middleton. (2007). Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25:2739-2749 (Pubitemid 350127858)
3. da Silva Meirelles L, PC Chagastelles and NB Nardi. (2006). Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119:2204-2213 (Pubitemid 43960310)
4. Uccelli A, L Moretta and V Pistoia. (2008). Mesenchymal stem cells in health and disease. Nat Rev Immunol 8:726-736
5. Zhao S, R Wehner, M Bornhauser, R Wassmuth, M Bachmann and M Schmitz. (2010). Immunomodulatory properties of mesenchymal stromal cells and their therapeutic consequences for immune-mediated disorders. Stem Cells Dev 19:607-614
6. Chateauvieux S, JL Ichante, B Delorme, V Frouin, G Pietu, A Langonne, N Gallay, L Sensebe, MT Martin, KA Moore and P Charbord. (2007). Molecular profile of mouse stromal mesenchymal stem cells. Physiol Genomics 29:128-138 (Pubitemid 46701994)
7. Jansen BJ, C Gilissen, H Roelofs, A Schaap-Oziemlak, JA Veltman, RA Raymakers, JH Jansen, G Kogler, CG Figdor, R Torensma and GJ Adema. (2010). Functional differences between mesenchymal stem cell populations are reflected by their transcriptome. Stem Cells Dev 19:481-490
8. Kaltz N, J Ringe, C Holzwarth, P Charbord, M Niemeyer, VR Jacobs, C Peschel, T Haupl and RA Oostendorp. (2010). Novel markers of mesenchymal stem cells defined by genome-wide gene expression analysis of stromal cells from different sources. Exp Cell Res 316:2609-2617
9. Tsai MS, SM Hwang, KD Chen, YS Lee, LW Hsu, YJ Chang, CN Wang, HH Peng, YL Chang, et al. (2007). Functional network analysis of the transcriptomes of mesenchymal stem cells derived from amniotic fluid, amniotic membrane, cord blood, and bone marrow. Stem Cells 25:2511-2523
10. Wagner W, F Wein, A Seckinger, M Frankhauser, U Wirkner, U Krause, J Blake, C Schwager, V Eckstein, W Ansorge and AD Ho. (2005). Comparative characteristics of mesenchymalstem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33:1402-1416 (Pubitemid 41541969)
11. Gaebel R, D Furlani, H Sorg, B Polchow, J Frank, K Bieback, W Wang, C Klopsch, LL Ong, et al. (2011). Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration. PLoS One 6:e15652
12. Kaewkhaw R, AM Scutt and JW Haycock. (2011). Anatomical site influences the differentiation of adipose-derived stem cells for Schwann-cell phenotype and function. Glia 59:734-749
13. Rebelatto CK, AM Aguiar, MP Moretao, AC Senegaglia, P Hansen, F Barchiki, J Oliveira, J Martins, C Kuligovski, et al. (2008). Dissimilar differentiation of mesenchymal stem cells from bone marrow, umbilical cord blood, and adipose tissue. Exp Biol Med (Maywood) 233:901-913
14. Takashima Y, T Era, K Nakao, S Kondo, M Kasuga, AG Smith and S Nishikawa. (2007). Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129:1377-1388 (Pubitemid 46970707)
15. Bianco P, PG Robey and PJ Simmons. (2008). Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2:313-319 (Pubitemid 351467394)
16. Javazon EH, KJ Beggs and AW Flake. (2004). Mesenchymal stem cells: paradoxes of passaging. Exp Hematol 32:414-425 (Pubitemid 38624325)
17. Peister A, JA Mellad, BL Larson, BM Hall, LF Gibson and DJ Prockop. (2004). Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103:1662-1668 (Pubitemid 38268957)
18. Hegyi B, B Sagi, J Kovacs, J Kiss, VS Urban, G Meszaros, E Monostori and F Uher. (2010). Identical, similar or different? Learning about immunomodulatory function ofmesenchymal stem cells isolated from various mouse tissues: bone marrow, spleen, thymus and aorta wall. Int Immunol 22:551-559
19. Dexter TM and NG Testa. (1976). Differentiation and proliferation of hemopoietic cells in culture. Methods Cell Biol 14:387-405 (Pubitemid 8001054)
20. Urban VS, J Kiss, J Kovacs, E Gocza, V Vas, E Monostori and F Uher. (2008). Mesenchymal stem cells cooperate with bone marrow cells in therapy of diabetes. Stem Cells 26:244-253
21. Shen B, D Bhargav, A Wei, LA Williams, H Tao, DD Ma and AD Diwan. (2009). BMP-13 emerges as a potential inhibitor of bone formation. Int J Biol Sci 5:192-200
22. Anjos-Afonso F and D Bonnet. (2007). Nonhematopoietic/ endothelial SSEA-1 + cells define the most primitive progenitors in the adult murine bone marrow mesenchymal compartment. Blood 109:1298-1306 (Pubitemid 46220683)
23. Gang EJ, D Bosnakovski, CA Figueiredo, JW Visser and RC Perlingeiro. (2007). SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 109:1743-1751 (Pubitemid 46239610)
24. Evans PM and C Liu. (2008). Roles of Krupel-like factor 4 in normal homeostasis, cancer and stem cells. Acta Biochim Biophys Sin (Shanghai) 40:554-564 (Pubitemid 352009081)
25. Minasi MG, M Riminucci, L De Angelis, U Borello, B Berarducci, A Innocenzi, A Caprioli, D Sirabella, M Baiocchi, et al. (2002). The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129:2773-2783 (Pubitemid 34874259)
26. Wardle FC and VE Papaioannou. (2008). Teasing out T-box targets in early mesoderm. Curr Opin Genet Dev 18:418-425 (Pubitemid 50310296)
27. Wang KC, JA Helms and HY Chang. (2009). Regeneration, repair and remembering identity: the three Rs of Hox gene expression. Trends Cell Biol 19:268-275
28. Beverdam A and F Meijlink. (2001). Expression patterns of group-I aristaless-related genes during craniofacial and limb development. Mech Dev 107:163-167 (Pubitemid 32755814)
29. Buckingham M and F Relaix. (2007). The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu Rev Cell Dev Biol 23:645-673
30. Lagha M, S Brunelli, G Messina, A Cumano, T Kume, F Relaix and ME Buckingham. (2009). Pax3:Foxc2 reciprocal repression in the somite modulates muscular versus vascular cell fate choice in multipotent progenitors. Dev Cell 17:892-899
31. Sansregret L and A Nepveu. (2008). The multiple roles of CUX1: insights from mouse models and cell-based assays. Gene 412:84-94
32. Kraus P and T Lufkin. (2006). Dlx homeobox gene control of mammalian limb and craniofacial development. Am J Med Genet A 140:1366-1374 (Pubitemid 43993127)
33. Anderson DM, J Arredondo, K Hahn, G Valente, JF Martin, J Wilson-Rawls and A Rawls. (2006). Mohawk is a novel homeobox gene expressed in the developing mouse embryo. Dev Dyn 235:792-801
34. Ito Y, N Toriuchi, T Yoshitaka, H Ueno-Kudoh, T Sato, S Yokoyama, K Nishida, T Akimoto, M Takahashi, S Miyaki and H Asahara. (2010). The Mohawk homeobox gene is a critical regulator of tendon differentiation. Proc Natl Acad Sci U S A 107:10538-10542
35. Kumar JP. (2009). The sine oculis homeobox (SIX) family of transcription factors as regulators of development and disease. Cell Mol Life Sci 66:565-583
36. Chapman DL, N Garvey, S Hancock, M Alexiou, SI Agulnik, JJ Gibson-Brown, J Cebra-Thomas, RJ Bollag, LM Silver and E Papaioannou. (1996). Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev Dyn 206:379-390 (Pubitemid 26260172)
37. Kanzler B and TN Dear. (2001). Hox11 acts cell autonomously in spleen development and its absence results in altered cell fate of mesenchymal spleen precursors. Dev Biol 234:231-243 (Pubitemid 32477037)
38. Brendolan A, MM Rosado, R Carsetti, L Selleri and TN Dear. (2007). Development and function of the mammalian spleen. Bioessays 29:166-177 (Pubitemid 46340251)
39. Meijlink F, A Beverdam, A Brouwer, TC Oosterveen and DT Berge. (1999). Vertebrate aristaless-related genes. Int J Dev Biol 43:651-663
40. Lengner CJ, FD Camargo, K Hochedlinger, GG Welstead, S Zaidi, S Gokhale, HR Scholer, A Tomilin and R Jaenisch. (2007). Oct4 expression is not required for mouse somatic stem cell self-renewal. Cell Stem Cell 1:403-415 (Pubitemid 47506536)
41. Menicanin D, PM Bartold, AC Zannettino and S Gronthos. (2009). Genomic profiling of mesenchymal stem cells. Stem Cell Rev 5:36-50
42. Suzuki E, T Evans, J Lowry, L Truong, DW Bell, JR Testa and K Walsh. (1996). The human GATA-6 gene: structure, chromosomal location, and regulation of expression by tissue-specific and mitogen-responsive signals. Genomics 38:283-290 (Pubitemid 27030116)
43. Kubo H, M Shimizu, Y Taya, T Kawamoto, M Michida, E Kaneko, A Igarashi, M Nishimura, K Segoshi, et al. (2009). Identification of mesenchymal stem cell (MSC)-transcription factors by microarray and knockdown analyses, and signature molecule-marked MSC in bone marrow by immunohistochemistry. Genes Cells 14:407-424
44. Watt AJ, R Zhao, J Li and SA Duncan. (2007). Development of the mammalian liver and ventral pancreas is dependent on GATA4. BMC Dev Biol 7:37
45. Riazi AM, JK Takeuchi, LK Hornberger, SH Zaidi, F Amini, J Coles, BG Bruneau and GS Van Arsdell. (2009). NKX2-5 regulates the expression of beta-catenin and GATA4 in ventricular myocytes. PLoS One 4:e5698
46. Morikawa S, Y Mabuchi, K Niibe, S Suzuki, N Nagoshi, T Sunabori, S Shimmura, Y Nagai, T Nakagawa, H Okano and Y Matsuzaki. (2009). Development of mesenchymal stem cells partially originate from the neural crest. Biochem Biophys Res Commun 379:1114-1119
47. Lagha M, T Sato, B Regnault, A Cumano, A Zuniga, J Licht, F Relaix and M Buckingham. (2010). Transcriptome analyses based on genetic screens for Pax3 myogenic targets in the mouse embryo. BMC Genomics 11:696
48. Ando Z, S Sato, K Ikeda and K Kawakami. (2005). Slc12a2 is a direct target of two closely related homeobox proteins, Six1 and Six4. FEBS J 272:3026-3041. (Pubitemid 40904690)
49. Ford HL. (1998). Homeobox genes: a link between development, cell cycle, and cancer? Cell Biol Int 22:397-400 (Pubitemid 29238051)
50. Anderson DM, BJ Beres, J Wilson-Rawls and A Rawls. (2009). The homeobox gene Mohawk represses transcription by recruiting the sin3A/HDAC co-repressor complex. Dev Dyn 238:572-580
51. Esner M, SM Meilhac, F Relaix, JF Nicolas, G Cossu and ME Buckingham. (2006). Smooth muscle of the dorsal aorta shares a common clonal origin with skeletal muscle of the myotome. Development 133:737-749
52. Wasteson P, BR Johansson, T Jukkola, S Breuer, LM Akyurek, J Partanen and P Lindahl. (2008). Developmental origin of smooth muscle cells in the descending aorta in mice. Development 135:1823-1832
53. Pouget C, K Pottin and T Jaffredo. (2008). Sclerotomal origin of vascular smooth muscle cells and pericytes in the embryo. Dev Biol 315:437-447
54. Ackema KB and J Charite. (2008). Mesenchymal stem cells from different organs are characterized by distinct topographic Hox codes. Stem Cells Dev 17:979-991
55. Chang HY, JT Chi, S Dudoit, C Bondre, M van de Rijn, D Botstein and PO Brown. (2002). Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci U S A 99:12877-12882
56. Chi JT, EH Rodriguez, Z Wang, DS Nuyten, S Mukherjee, M van de Rijn, MJ van de Vijver, T Hastie and PO Brown. (2007). Gene expression programs of human smooth muscle cells: tissue-specific differentiation and prognostic significance in breast cancers. PLoS Genet 3:1770-1784 (Pubitemid 47510268)
57. Gesta S, M Bluher, Y Yamamoto, AW Norris, J Berndt, S Kralisch, J Boucher, C Lewis and CR Kahn. (2006). Evidence for a role of developmental genes in the origin of obesity and body fat distribution. Proc Natl Acad Sci U S A 103:6676-6681
58. Creuzet S, G Couly, C Vincent and NM Le Douarin. (2002). Negative effect of Hox gene expression on the development of the neural crest-derived facial skeleton. Development 129:4301-4313
59. Leucht P, JB Kim, R Amasha, AW James, S Girod and JA Helms. (2008). Embryonic origin and Hox status determine progenitor cell fate during adult bone regeneration. Development 135:2845-2854
60. Revest JM, RK Suniara, K Kerr, JJ Owen and C Dickson. (2001). Development of the thymus requires signaling through the fibroblast growth factor receptor R2-IIIb. J Immunol 167:1954-1961 (Pubitemid 32747500)
61. Ahn DG, MJ Kourakis, LA Rohde, LM Silver and RK Ho. (2002). T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature 417:754-758 (Pubitemid 34640630)
62. Agarwal P, JN Wylie, J Galceran, O Arkhitko, C Li, C Deng, R Grosschedl and BG Bruneau. (2003). Tbx5 is essential for forelimb bud initiation following patterning of the limb field in the mouse embryo. Development 130:623-633 (Pubitemid 36231280)
63. Li QY, RA Newbury-Ecob, JA Terrett, DI Wilson, AR Curtis, CH Yi, T Gebuhr, PJ Bullen, SC Robson, et al. (1997). Holt Oram syndrome is caused by mutations in TBX5, a member of the Brachyury (T) gene family. Nat Genet 15:21-29 (Pubitemid 27014945)
64. Holmberg J, G Ingner, C Johansson, P Leander and TA Hjalt. (2008). PITX2 gain-of-function induced defects in mouse forelimb development. BMC Dev Biol 8:25
65. Qu S, SC Tucker, Q Zhao, B deCrombrugghe and R Wisdom. (1999). Physical and genetic interactions between Alx4 and Cart1. Development 126:359-369 (Pubitemid 29083973)
66. Roberts CW, JR Shutter and SJ Korsmeyer. (1994). Hox11 controls the genesis of the spleen. Nature 368:747-749 (Pubitemid 24153415)
67. Hu B, YM Wu, Z Wu and SH Phan. (2010). Nkx2.5/Csx represses myofibroblast differentiation. Am J Respir Cell Mol Biol 42:218-226
68. Sarnat HB, DR Benjamin, JR Siebert, GB Kletter and SR Cheyette. (2002). Agenesis of the mesencephalon and metencephalon with cerebellar hypoplasia: putative mutation in the EN2 gene-report of 2 cases in early infancy. Pediatr Dev Pathol 5:54-68 (Pubitemid 34279699)
69. Herrup K, C Murcia, F Gulden, B Kuemerle and N Bilovocky. (2005). The genetics of early cerebellar development: networks not pathways. Prog Brain Res 148:21-27
70. Chang SC, B Hoang, JT Thomas, S Vukicevic, FP Luyten, NJ Ryba, CA Kozak, AH Reddi and M Moos, Jr. (1994). Cartilage-derived morphogenetic proteins. New members of the transforming growth factor-beta superfamily predominantly expressed in long bones during human embryonic development. J Biol Chem 269:28227-28234
71. Bobacz K, R Gruber, A Soleiman, WB Graninger, FP Luyten and L Erlacher. (2002). Cartilage-derived morphogenetic protein-1 and -2 are endogenously expressed in healthy and osteoarthritic human articular chondrocytes and stimulate matrix synthesis. Osteoarthritis Cartilage 10:394-401. (Pubitemid 34662374)
72. Tassabehji M, ZM Fang, EN Hilton, J McGaughran, Z Zhao, CE de Bock, E Howard, M Malass, D Donnai, et al. (2008). Mutations in GDF6 are associated with vertebral segmentation defects in Klippel-Feil syndrome. Hum Mutat 29:1017-1027
73. Settle SH, Jr., RB Rountree, A Sinha, A Thacker, K Higgins and DM Kingsley. (2003). Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse Gdf6 and Gdf5 genes. Dev Biol 254:116-130 (Pubitemid 36259876)
74. Vieira NM, E Zucconi, CR Bueno, Jr., M Secco, MF Suzuki, P Bartolini, M Vainzof and M Zatz. (2010). Human multipotent mesenchymal stromal cells from distinct sources show different in vivo potential to differentiate into muscle cells when injected in dystrophic mice. Stem Cell Rev 6:560-566
75. Badri L, NM Walker, T Ohtsuka, Z Wang, M Delmar, A Flint, M Peters-Golden, GB Toews, DJ Pinsky, PH Krebsbach and VN Lama. (2011). Epithelial interactions and local engraftment of lung-resident mesenchymal stem cells. Am J Respir Cell Mol Biol 45:809-816
76. Karp JM and GS Leng Teo. (2009). Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4:206-216