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Dermal Precursors and the Origins of the Wound Fibroblast

  • Jeffrey M. DavidsonEmail author
Conference paper
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Part of the NATO Science for Peace and Security Series A: Chemistry and Biology book series (NAPSA)

Abstract

Tissue repair demands the efficient restoration of connective tissue integrity and architecture. The brunt of the task falls on the fibroblast, a cell type strongly committed to the production of extracellular matrix. Recent investigation has refined the historical concept that the bone marrow and circulating precursors can make a significant, transient contribution to wound healing during the formation of granulation tissue. In parallel, there is mounting evidence that a subset of dermal mesenchymal cells have pluripotent properties that could contribute to the restoration and even regeneration of wound sites. The interrelationships between mesenchymal stem cells, circulating fibrocytes, and dermal progenitors are still an evolving area of investigation. Nevertheless, the manipulation of these cell types for wound healing and tissue engineering applications is a promising strategy.

Keywords

Wound healing mesenchymal stem cell fibrocyte progenitor 
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Notes

Acknowledgements

The author is grateful to Pampee P. Young, Susan R. Opalenik, and Mariagabriella Giro for their contributions to this work. Supported by the Department of Veterans Affairs and NIH grants AG06528 and AR041943.

References

  1. Abe R et al (2001) Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. J Immunol 166(12):7556–7562Google Scholar
  2. Abraham DJ et al (2007) New developments in fibroblast and myofibroblast biology: implications for fibrosis and scleroderma. Curr Rheumatol Rep 9(2):136–143CrossRefGoogle Scholar
  3. Ahmed N, Stanford WL, Kandel RA (2007) Mesenchymal stem and progenitor cells for cartilage repair. Skeletal Radiol 36(10):909–912CrossRefGoogle Scholar
  4. Alfaro MP et al (2009) The Wnt modulator sFRP2 enhances mesenchymal stem cell engraftment, granulation tissue formation and myocardial repair. Proc Natl Acad Sci USA 105:18366–18371CrossRefGoogle Scholar
  5. Allgower M, Hulliger L (1960) Origin of fibroblasts from mononucelar blood cells: a study on the in vitro formation of the collagen precursor, hydroxyproline, in buffy coat cultures. Surgery 47:603–609Google Scholar
  6. Asahara T et al (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302):964–967CrossRefGoogle Scholar
  7. Asahara T et al (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85(3):221–228CrossRefGoogle Scholar
  8. Badiavas EV et al (2003) Participation of bone marrow derived cells in cutaneous wound healing. J Cell Physiol 196(2):245–250CrossRefGoogle Scholar
  9. Bartsch G et al (2005) Propagation, expansion, and multilineage differentiation of human somatic stem cells from dermal progenitors. Stem Cells Dev 14(3):337–348CrossRefGoogle Scholar
  10. Bedelbaeva K et al (2010) Lack of p21 expression links cell cycle control and appendage regeneration in mice. Proc Nat Acad Sci USA 107:5845–5850CrossRefGoogle Scholar
  11. Bellini A, Mattoli S (2007) The role of the fibrocyte, a bone marrow-derived mesenchymal progenitor, in reactive and reparative fibroses. Lab Invest 87(9):858–870CrossRefGoogle Scholar
  12. Bucala R (2008) Circulating fibrocytes: cellular basis for NSF. J Am Coll Radiol 5(1):36–39CrossRefGoogle Scholar
  13. Bucala R et al (1994) Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Mol Med 1(1):71–81Google Scholar
  14. Caldwell RL et al (2008) Tissue profiling MALDI mass spectrometry reveals prominent calcium-binding proteins in the proteome of regenerative MRL mouse wounds. Wound Repair Regen 16:442–449CrossRefGoogle Scholar
  15. Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9(5):641–650CrossRefGoogle Scholar
  16. Caplan AI (1994) The mesengenic process. Clin Plast Surg 21(3):429–435Google Scholar
  17. Caplan AI (2007) Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213(2):341–347CrossRefGoogle Scholar
  18. Ceradini DJ, Gurtner GC (2005) Homing to hypoxia: HIF-1 as a mediator of progenitor cell recruitment to injured tissue. Trends Cardiovasc Med 15(2):57–63CrossRefGoogle Scholar
  19. Cha J, Falanga V (2007) Stem cells in cutaneous wound healing. Clin Dermatol 25(1):73–78CrossRefGoogle Scholar
  20. Chen FG et al (2007) Clonal analysis of nestin vimentin + multipotent fibroblasts isolated from human dermis. J Cell Sci 120(Pt 16):2875–2883CrossRefGoogle Scholar
  21. Chesney J et al (1997) The peripheral blood fibrocyte is a potent antigen-presenting cell capable of priming naive T cells in situ. Proc Natl Acad Sci USA 94(12):6307–6312CrossRefGoogle Scholar
  22. Chunmeng S, Tianmin C (2004) Skin: a promising reservoir for adult stem cell populations. Med Hypotheses 62(5):683–688CrossRefGoogle Scholar
  23. Cohnheim J (1867) Ueber Entzundung und Eiterung. Path Anat Physiol Klin Med 40:1–79Google Scholar
  24. Cotsarelis G (2006) Epithelial stem cells: a folliculocentric view. J Invest Dermatol 126(7):1459–1468CrossRefGoogle Scholar
  25. Crigler L et al (2007) Isolation of a mesenchymal cell population from murine dermis that contains progenitors of multiple cell lineages. FASEB J 21(9):2050–2063CrossRefGoogle Scholar
  26. Davis TA, Lennon G (2005) Mice with a regenerative wound healing capacity and an SLE autoimmune phenotype contain elevated numbers of circulating and marrow-derived macrophage progenitor cells. Blood Cells Mol Dis 34(1):17–25CrossRefGoogle Scholar
  27. De Bari C, Dell’accio F (2007) Mesenchymal stem cells in rheumatology: a regenerative approach to joint repair. Clin Sci (Lond) 113(8):339–348CrossRefGoogle Scholar
  28. Delo DM et al (2006) Amniotic fluid and placental stem cells. Methods Enzymol 419:426–438CrossRefGoogle Scholar
  29. Dennis JE et al (2002) The STRO-1+ marrow cell population is multipotential. Cells Tissues Organs 170(2–3):73–82CrossRefGoogle Scholar
  30. Dicker A et al (2005) Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp Cell Res 308(2):283–290CrossRefGoogle Scholar
  31. Eguchi M, Masuda H, Asahara T (2007) Endothelial progenitor cells for postnatal vasculogenesis. Clin Exp Nephrol 11(1):18–25CrossRefGoogle Scholar
  32. Falanga V (2004) The chronic wound: impaired healing and solutions in the context of wound bed preparation. Blood Cells Mol Dis 32(1):88–94CrossRefGoogle Scholar
  33. Falanga V et al (2007) Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng 13(6):1299–1312CrossRefGoogle Scholar
  34. Fathke C et al (2004) Contribution of bone marrow-derived cells to skin: collagen deposition and wound repair. Stem Cells 22(5):812–822CrossRefGoogle Scholar
  35. Fernandes KJ et al (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6(11):1082–1093CrossRefGoogle Scholar
  36. Fernandes KJ et al (2006) Analysis of the neurogenic potential of multipotent skin-derived precursors. Exp Neurol 201(1):32–48CrossRefGoogle Scholar
  37. Fernandes KJ, Toma JG, Miller FD (2008) Multipotent skin-derived precursors: adult neural crest-related precursors with therapeutic potential. Philos Trans R Soc Lond B Biol Sci 363:185–198CrossRefGoogle Scholar
  38. Friedenstein AJ (1995) Marrow stromal fibroblasts. Calcif Tissue Int 56(Suppl 1):S17Google Scholar
  39. Friedenstein A, Kuralesova AI (1971) Osteogenic precursor cells of bone marrow in radiation chimeras. Transplantation 12(2):99–108CrossRefGoogle Scholar
  40. Friedenstein AJ et al (1974) Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 2(2):83–92Google Scholar
  41. Gharzi A, Reynolds AJ, Jahoda CA (2003) Plasticity of hair follicle dermal cells in wound healing and induction. Exp Dermatol 12(2):126–136CrossRefGoogle Scholar
  42. Gronthos S et al (1994) The STRO-1+ fraction of adult human bone marrow contains the osteogenic precursors. Blood 84(12):4164–4173Google Scholar
  43. Gurtner GC, Callaghan MJ, Longaker MT (2007) Progress and potential for regenerative medicine. Annu Rev Med 58:299–312CrossRefGoogle Scholar
  44. Heber-Katz E et al (2004) Spallanzani’s mouse: a model of restoration and regeneration. Curr Top Microbiol Immunol 280:165–189CrossRefGoogle Scholar
  45. Hennessy B, Korbling M, Estrov Z (2004) Circulating stem cells and tissue repair. Panminerva Med 46(1):1–11Google Scholar
  46. Hoogduijn MJ, Gorjup E, Genever PG (2006) Comparative characterization of hair follicle dermal stem cells and bone marrow mesenchymal stem cells. Stem Cells Dev 15(1):49–60CrossRefGoogle Scholar
  47. Hunt DP et al (2008) A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells 26(1):163–172CrossRefGoogle Scholar
  48. Ishii G et al (2005) In vivo characterization of bone marrow-derived fibroblasts recruited into fibrotic lesions. Stem Cells 23(5):699–706CrossRefGoogle Scholar
  49. Iwano M et al (2002) Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110(3):341–350Google Scholar
  50. Jahoda CA et al (2003) Hair follicle dermal cells differentiate into adipogenic and osteogenic lineages. Exp Dermatol 12(6):849–859CrossRefGoogle Scholar
  51. Kim WS et al (2007) Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts. J Dermatol Sci 48(1):15–24CrossRefGoogle Scholar
  52. Lako M et al (2002) Hair follicle dermal cells repopulate the mouse haematopoietic system. J Cell Sci 115(Pt 20):3967–3974CrossRefGoogle Scholar
  53. Lama VN, Phan SH (2006) The extrapulmonary origin of fibroblasts: stem/progenitor cells and beyond. Proc Am Thorac Soc 3(4):373–376CrossRefGoogle Scholar
  54. Le Blanc K, Pittenger M (2005) Mesenchymal stem cells: progress toward promise. Cytotherapy 7(1):36–45Google Scholar
  55. Li X et al (2001) Genetic control of the rate of wound healing in mice. Heredity 86(Pt 6):668–674CrossRefGoogle Scholar
  56. Li WW et al. (2005) The role of therapeutic angiogenesis in tissue repair and regeneration. Adv Skin Wound Care 18(9):491–500; quiz 501–502CrossRefGoogle Scholar
  57. Lindblad WJ (1998) Perspective article: collagen expression by novel cell populations in the dermal wound environment. Wound Repair Regen 6(3):186–193CrossRefGoogle Scholar
  58. Lindblad WJ et al (1987) Induction of prolyl hydroxylase activity in a nonadherent population of human leukocytes. Biochem Biophys Res Commun 147(1):486–493CrossRefGoogle Scholar
  59. Lowry WE et al (2008) Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci USA 105(8):2883–2888CrossRefGoogle Scholar
  60. Maherali N et al (2007) Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 1(1):55–70CrossRefGoogle Scholar
  61. McClain SA et al (1996) Mesenchymal cell activation is the rate-limiting step of granulation tissue induction. Am J Pathol 149(4):1257–1270Google Scholar
  62. Okada H, Kalluri R (2005) Cellular and molecular pathways that lead to progression and regression of renal fibrogenesis. Curr Mol Med 5(5):467–474CrossRefGoogle Scholar
  63. Okada H et al (1997) Early role of Fsp1 in epithelial-mesenchymal transformation. Am J Physiol 273(4 Pt 2):F563–F574Google Scholar
  64. Opalenik SR, Davidson JM (2005) Fibroblast differentiation of bone marrow-derived cells during wound repair. FASEB J 19(11):1561–1563Google Scholar
  65. Paget J (1863) Lectures on surgical pathology. Longmans, London, p 848Google Scholar
  66. Peng H, Huard J (2004) Muscle-derived stem cells for musculoskeletal tissue regeneration and repair. Transpl Immunol 12(3–4):311–319CrossRefGoogle Scholar
  67. Pereira RF et al (1998) Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta. Proc Natl Acad Sci USA 95(3):1142–1147CrossRefGoogle Scholar
  68. Pilling D et al (2003) Inhibition of fibrocyte differentiation by serum amyloid P. J Immunol 171(10):5537–5546Google Scholar
  69. Pittenger MF et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411):143–147CrossRefGoogle Scholar
  70. Ponte AL et al (2007) The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 25(7):1737–1745CrossRefGoogle Scholar
  71. Prichard HL, Reichert WM, Klitzman B (2007) Adult adipose-derived stem cell attachment to biomaterials. Biomaterials 28(6):936–946CrossRefGoogle Scholar
  72. Quan TE et al (2004) Circulating fibrocytes: collagen-secreting cells of the peripheral blood. Int J Biochem Cell Biol 36(4):598–606CrossRefGoogle Scholar
  73. Quan TE, Cowper SE, Bucala R (2006) The role of circulating fibrocytes in fibrosis. Curr Rheumatol Rep 8(2):145–150CrossRefGoogle Scholar
  74. Richardson GD et al (2005) Plasticity of rodent and human hair follicle dermal cells: implications for cell therapy and tissue engineering. J Investig Dermatol Symp Proc 10(3):180–183CrossRefGoogle Scholar
  75. Richter W (2007) Cell-based cartilage repair: illusion or solution for osteoarthritis. Curr Opin Rheumatol 19(5):451–456Google Scholar
  76. Roh C, Lyle S (2006) Cutaneous stem cells and wound healing. Pediatr Res 59(4 Pt 2):100R–103RCrossRefGoogle Scholar
  77. Sieber-Blum M et al (2004) Pluripotent neural crest stem cells in the adult hair follicle. Dev Dyn 231(2):258–269CrossRefGoogle Scholar
  78. Simmons PJ, Torok-Storb B (1991) Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 78(1):55–62Google Scholar
  79. Stewart K et al (2003) STRO-1, HOP-26 (CD63), CD49a and SB-10 (CD166) as markers of primitive human marrow stromal cells and their more differentiated progeny: a comparative investigation in vitro. Cell Tissue Res 313(3):281–290CrossRefGoogle Scholar
  80. Stirling G, Kakkar V (1969) Cells in the circulating blood capable of producing connective tissue. Br J Exp Pathol 50:51–55Google Scholar
  81. Toma JG et al (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3(9):778–784CrossRefGoogle Scholar
  82. Toma JG et al (2005) Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23(6):727–737CrossRefGoogle Scholar
  83. Wang JF et al (2007) Fibrocytes from burn patients regulate the activities of fibroblasts. Wound Repair Regen 15(1):113–121CrossRefGoogle Scholar
  84. Yamanaka S (2008) Induction of pluripotent stem cells from mouse fibroblasts by four transcription factors. Cell Prolif 41(Suppl 1):51–56Google Scholar
  85. Yang L et al (2002) Peripheral blood fibrocytes from burn patients: identification and quantification of fibrocytes in adherent cells cultured from peripheral blood mononuclear cells. Lab Invest 82(9):1183–1192Google Scholar
  86. Young HE et al (1993) Pluripotent mesenchymal stem cells reside within avian connective tissue matrices. In Vitro Cell Dev Biol Anim 29A(9):723–736CrossRefGoogle Scholar
  87. Young HE et al (1995) Mesenchymal stem cells reside within the connective tissues of many organs. Dev Dyn 202(2):137–144CrossRefGoogle Scholar
  88. Young HE et al (2001) Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat Rec 264(1):51–62CrossRefGoogle Scholar
  89. Yu H et al (2007) Mouse chromosome 9 quantitative trait loci for soft tissue regeneration: congenic analysis and fine mapping. Wound Repair Regen 15(6):922–927CrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of PathologyVanderbilt University School of MedicineNashvilleUSA
  2. 2.Research Service, VA Tennessee Valley Healthcare SystemNashvilleUSA

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