HOX and TALE signatures specify human stromal stem cell populations from different sources

Journal of Cellular Physiology

Volumn 228, Issue 4, 2013, Pages 879-889

  Picchi, Jacopo ^a   Trombi, Luisa ^b   Spugnesi, Laura ^a   Barachini, Serena ^b   Maroni, Giorgia ^a   Brodano, Giovanni Barbanti ^c   Boriani, Stefano ^c   Valtieri, Mauro ^d,e   Petrini, Mario ^b   Magli, Maria Cristina ^a  

^a CNR   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^d ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^e Temple University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; HOX PROTEIN; PROTEIN TALE; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL ISOLATION; CELL POPULATION; CONTROLLED STUDY; DNA BINDING; HUMAN; HUMAN CELL; HUMAN TISSUE; ILIAC CREST; IMMUNOPHENOTYPING; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL; STERNUM; STROMA CELL; TOOTH PULP;

BONE MARROW CELLS; CELL DIFFERENTIATION; DENTAL PULP; GENE EXPRESSION; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; HUMANS; MESENCHYMAL STROMAL CELLS; STROMAL CELLS;

EID: 84871690211     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24239     Document Type: Article

References (64)

1. Ackema KB, Charitè J. 2008. Mesenchymal stem cells from different organs are characterized by distinct topographic Hox codes. Stem Cells Dev 17:979-991.
2. Bach C, Buhl S, Mueller D, Garcia-Cuellar MP, Maethner E, Slany RK. 2010. Leukemogenic transformation by HOXA cluster genes. Blood 115:2910-2918.
3. Bianco P, Robey PG, Simmons PJ. 2008. Mesenchymal stem cells: Revisiting history, concepts, and assays. Cell Stem Cell 2:313-319.
4. Bianco P, Robey PG, Saggio I, Riminucci M. 2010. "Mesenchymal" stem cells in human bone marrow (skeletal stem cells): A critical discussion of their nature, identity, and significance in incurable skeletal disease. Hum Gene Ther 21:1057-1066.
5. Caplan AI. 2007. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213:341-347.
6. Carapuco M, Novoa A, Bobola N, Mallo M. 2005. Hox genes specify vertebral types in the presomitic mesoderm. Genes Dev 19:2116-2121.
7. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, Botstein D, Brown PO. 2002. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA 99:12877-12882.
8. Couly G, Creuzet S, Bennaceur S, Vincent C, Le Douarin NM. 2002. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 129:1061-1073.
9. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Peault B. 2008. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301-313.
10. da Silva Meirelles L, Chagastelles PC, Nardi NB. 2006. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119:2204-2213.
11. da Silva Meirelles L, Caplan AI, Nardi NB. 2008. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26:2287-2299.
12. D'Anto V, Cantile M, D'Armiento M, Schiavo G, Spagnuolo G, Terracciano L, Vecchione R, Cillo C. 2006. The HOX genes are expressed, in vivo, in human tooth germs: In vitro cAMP exposure of dental pulp cells results in parallel HOX network activation and neuronal differentiation. J Cell Biochem 97:836-848.
13. Davidson AJ, Ernst P, Wang Y, Dekens MP, Kingsley PD, Palis J, Korsmeyer SJ, Daley GQ, Zon LI. 2003. cdx4 mutants fail to specify blood progenitors and can be rescued by multiple hox genes. Nature 425:300-306.
14. Delorme B, Ringe J, Pontikoglou C, Gaillard J, Langonne A, Sensebe L, Noel D, Jorgensen C, Haupl T, Charbord P. 2009. Specific lineage-priming of bone marrow mesenchymal stem cells provides the molecular framework for their plasticity. Stem Cells 27:1142-1151.
15. Di Rosa P, Villaescusa JC, Longobardi E, Iotti G, Ferretti E, Diaz VM, Miccio A, Ferrari G, Blasi F. 2007. The homeodomain transcription factor Prep1 (pKnox1) is required for hematopoietic stem and progenitor cell activity. Dev Biol 311:324-334.
16. Duboule D, Dolle P. 1989. The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J 8:1497-1505.
17. Dutta D, Umashankar M, Lewis EB, Rodrigues V, Vijayraghavan K. 2010. Hox genes regulate muscle founder cell pattern autonomously and regulate morphogenesis through motor neurons. J Neurogenet 24:95-108.
18. Ficara F, Murphy MJ, Lin M, Cleary ML. 2008. Pbx1 regulates self-renewal of long-term hematopoietic stem cells by maintaining their quiescence. Cell Stem Cell 2:484-496.
19. Gehring WJ, Hiromi Y. 1986. Homeotic genes and the homeobox. Annu Rev Genet 20:147-173.
20. Giordano A, Galderisi U, Marino IR. 2007. From the laboratory bench to the patient's bedside: An update on clinical trials with mesenchymal stem cells. J Cell Physiol 211:27-35.
21. Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, DenBesten P, Robey PG, Shi S. 2002. Stem cell properties of human dental pulp stem cells. J Dent Res 81:531-535.
22. Hassan MQ, Tare R, Lee SH, Mandeville M, Weiner B, Montecino M, van Wijnen AJ, Stein JL, Stein GS, Lian JB. 2007. HOXA10 controls osteoblastogenesis by directly activating bone regulatory and phenotypic genes. Mol Cell Biol 27:3337-3352.
23. He H, Hua X, Yan J. 2011. Epigenetic regulations in hematopoietic Hox code. Oncogene 30:379-388.
24. Holstege JC, de Graaff W, Hossaini M, Cano SC, Jaarsma D, van den Akker E, Deschamps J. 2008. Loss of Hoxb8 alters spinal dorsal laminae and sensory responses in mice. Proc Natl Acad Sci USA 105:6338-6343.
25. Huang GT, Gronthos S, Shi S. 2009. Mesenchymal stem cells derived from dental tissues vs. those from other sources: Their biology and role in regenerative medicine. J Dent Res 88:792-806.
26. Kogler G, Sensken S, Wernet P. 2006. Comparative generation and characterization of pluripotent unrestricted somatic stem cells with mesenchymal stem cells from human cord blood. Exp Hematol 34:1589-1595.
27. Kulterer B, Friedl G, Jandrositz A, Sanchez-Cabo F, Prokesch A, Paar C, Scheideler M, Windhager R, Preisegger KH, Trajanoski Z. 2007. Gene expression profiling of human mesenchymal stem cells derived from bone marrow during expansion and osteoblast differentiation. BMC Genomics 8:70.
28. Lappin TR, Grier DG, Thompson A, Halliday HL. 2006. HOX genes: Seductive science, mysterious mechanisms. Ulster Med J 75:23-31.
29. Lemischka IR. 2010. Hooking up with Oct4. Cell Stem Cell 6:291-292.
30. Leucht P, Kim JB, Amasha R, James AW, Girod S, Helms JA. 2008. Embryonic origin and Hox status determine progenitor cell fate during adult bone regeneration. Development 135:2845-2854.
31. Li C, Wong WH. 2001. Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31-36.
32. Liedtke S, Buchheiser A, Bosch J, Bosse F, Kruse F, Zhao X, Santourlidis S, Kogler G. 2010. The HOX Code as a "biological fingerprint" to distinguish functionally distinct stem cell populations derived from cord blood. Stem Cell Res 5:40-50.
33. Magli MC, Largman C, Lawrence HJ. 1997. Effects of HOX homeobox genes in blood cell differentiation. J Cell Physiol 173:168-177.
34. Mallo M, Magli MC. 2006. A look at life from the homeodomain. Workshop on homeodomain proteins, hematopoietic development and leukemias. EMBO Rep 7:976-980.
35. Mallo M, Wellik DM, Deschamps J. 2010. Hox genes and regional patterning of the vertebrate body plan. Dev Biol 344:7-15.
36. McGinnis W, Krumlauf R. 1992. Homeobox genes and axial patterning. Cell 68:283-302.
37. Menicanin D, Bartold PM, Zannettino AC, Gronthos S. 2009. Genomic profiling of mesenchymal stem cells. Stem Cell Rev 5:36-50.
38. Moens CB, Selleri L. 2006. Hox cofactors in vertebrate development. Dev Biol 291:193-206.
39. Morgan R. 2006. Hox genes: A continuation of embryonic patterning? Trends Genet 22:67-69.
40. Nauta AJ, Fibbe WE. 2007. Immunomodulatory properties of mesenchymal stromal cells. Blood 110:3499-3506.
41. Nesti C, Pardini C, Barachini S, D'Alessandro D, Siciliano G, Murri L, Petrini M, Vaglini F. 2011. Human dental pulp stem cells protect mouse dopaminergic neurons against MPP+ or rotenone. Brain Res 1367:94-102.
42. Pacini S, Carnicelli V, Trombi L, Montali M, Fazzi R, Lazzarini E, Giannotti S, Petrini M. 2010. Constitutive expression of pluripotency-associated genes in mesodermal progenitor cells (MPCs). PLoS ONE 5:e9861.
43. Petrini M, Pacini S, Trombi L, Fazzi R, Montali M, Ikehara S, Abraham NG. 2009. Identification and purification of mesodermal progenitor cells from human adult bone marrow. Stem Cells Dev 18:857-866.
44. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
45. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
46. Prockop DJ. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74.
47. Russell KC, Phinney DG, Lacey MR, Barrilleaux BL, Meyertholen KE, O'Connor KC. 2010. In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells 28:788-798.
48. Sarno JL, Kliman HJ, Taylor HS. 2005. HOXA10, Pbx2, and Meis1 protein expression in the human endometrium: Formation of multimeric complexes on HOXA10 target genes. J Clin Endocrinol Metab 90:522-528.
49. Schyr RB, Shabtai Y, Shashikant CS, Fainsod A. 2012. Cdx1 is essential for the initiation of HoxC8 expression during early embryogenesis. FASEB J 26:2674-2684.
50. Shah N, Sukumar S. 2010. The Hox genes and their roles in oncogenesis. Nat Rev Cancer 10:361-371.
51. Signore M, Cerio AM, Boe A, Pagliuca A, Zaottini V, Schiavoni L, Fedele G, Petti S, Navarra S, Ausiello CM, Pelosi E, Fatica A, Sorrentino A, Valtieri M. 2012. Identity and ranking of colonic mesenchymal stromal cells. J Cell Physiol 227:3291-3300.
52. Sorrentino A, Ferracin M, Castelli G, Biffoni M, Tomaselli G, Baiocchi M, Fatica A, Negrini M, Peschle C, Valtieri M. 2008. Isolation and characterization of CD146+ multipotent mesenchymal stromal cells. Exp Hematol 36:1035-1046.
53. Soshnikova N, Duboule D. 2008. Epigenetic regulation of Hox gene activation: The waltz of methyls. BioEssays 30:199-202.
54. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta L. 2008. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: Role of indoleamine 2, 3-dioxygenase and prostaglandin E2. Blood 111:1327-1333.
55. Takahashi Y, Hamada J, Murakawa K, Takada M, Tada M, Nogami I, Hayashi N, Nakamori S, Monden M, Miyamoto M, Katoh H, Moriuchi T. 2004. Expression profiles of 39 HOX genes in normal human adult organs and anaplastic thyroid cancer cell lines by quantitative real-time RT-PCR system. Exp Cell Res 293:144-153.
56. Trombi L, Pacini S, Montali M, Fazzi R, Chiellini F, Ikehara S, Petrini M. 2009. Selective culture of mesodermal progenitor cells. Stem Cells Dev 18:1227-1234.
57. Valtieri M, Sorrentino A. 2008. The mesenchymal stromal cell contribution to homeostasis. J Cell Physiol 217:296-300.
58. van der Hoeven F, Zakany J, Duboule D. 1996. Gene transpositions in the HoxD complex reveal a hierarchy of regulatory controls. Cell 85:1025-1035.
59. Villaescusa JC, Buratti C, Penkov D, Mathiasen L, Planaguma J, Ferretti E, Blasi F. 2009. Cytoplasmic Prep1 interacts with 4EHP inhibiting Hoxb4 translation. PLoS ONE 4:e5213.
60. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD. 2005. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33:1402-1416.
61. Wang KC, Helms JA, Chang HY. 2009. Regeneration, repair and remembering identity: The three Rs of Hox gene expression. Trends Cell Biol 19:268-275.
62. Wheadon H, Ramsey JM, Dobbin E, Dickson GJ, Corrigan PM, Freeburn RW, Thompson A. 2011. Differential Hox expression in murine embryonic stem cell models of normal and malignant hematopoiesis. Stem Cells Dev 20:1465-1476.
63. Yamamoto M, Takai D, Yamamoto F. 2003. Comprehensive expression profiling of highly homologous 39 hox genes in 26 different human adult tissues by the modified systematic multiplex RT-PCR method reveals tissue-specific expression pattern that suggests an important role of chromosomal structure in the regulation of hox gene expression in adult tissues. Gene Expr 11:199-210.
64. Zhao S, Wehner R, Bornhauser M, Wassmuth R, Bachmann M, Schmitz M. 2010. Immunomodulatory properties of mesenchymal stromal cells and their therapeutic consequences for immune-mediated disorders. Stem Cells Dev 19:607-614.