Skip to main content

Advertisement

SpringerLink
Log in

Multiple sources of non-embryonic multipotent stem cells: processed lipoaspirates and dermis as promising alternatives to bone-marrow-derived cell therapies

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

A body of evidence points to the existence of stem cell stores in adult tissues, in addition to the well-known hematopoietic stem cells from bone marrow. Many reports describe the ability of these multipotent cells (developmentally non-compromised with their organs of origin) to give rise to many different cell types in response to specific stimuli. This apparent plasticity provides new perspectives in tissue engineering and suggests the usefulness of these cells in future protocols of autologous transplantation, gene therapy, and tissue reconstitution in a number of pathological processes. Lipoaspirates and dermis represent accessible sources for obtaining such cells, with minimal discomfort to the donor, and might be promising candidates for cell therapy procedures once their features are experimentally accessed. The intention of the present work has been to gather reports on the phenotypic characteristics, profile, and plastic potential of these stem cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ADSCs:

adipose-derived stem cells

BM:

bone marrow

HSCs:

hematopoietic stem cells

MSCs:

mesenchymal stem cells

PBSC:

peripheral blood stem cells (HSCs mobilized from BM by cytokine injection)

PLAs:

processed lipoaspirates

SKPs:

skin-derived precursors

SVF:

stroma-vascular fraction from lipoaspirates

TCSCs:

tissue-committed stem cells

USSCs:

umbilical cord blood-derived unrestricted somatic stem cells

References

  • Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, Giordano FJ (2004) Stromal cell-derived factor-1a plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110:3300–3305

    Article  PubMed  Google Scholar 

  • Abedi M, Greer DA, Colvin GA, Demers DA, Dooner MS, Harpel JA, Weier H-U, Lambert J-F, Quesenberry PJ (2004) Robust conversion of marrow cells to skeletal muscle with formation of marrow-derived muscle cell colonies: a multifactorial process. Exp Hematol 32:426–434

    Article  PubMed  CAS  Google Scholar 

  • Allers C, Sierralta WD, Neubauer S, Rivera F, Minguell JJ, Congest PA (2004) Dynamic distribution of human bone marrow-derived mesenchymal stem cells after transplantation into adult unconditioned mice. Transplantation 78:503–508

    Article  PubMed  Google Scholar 

  • Almeida-Porada G, Porada CD, Tran N, Zanjani ED (2000) Cotransplantation of human stromal cell progenitors into preimmune fetal sheep results in early appearance of human donor cells in circulation and boosts cell levels in bone marrow at later time points after transplantation. Blood 95:3620–3627

    PubMed  CAS  Google Scholar 

  • Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Builla A (2003) Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425:968–973

    Article  PubMed  CAS  Google Scholar 

  • Arroyo AG, Yang JT, Rayburn H, Hynes RO (1996) Differential requirements for alpha4 integrins during fetal and adult hematopoieses. Cell 85:997–1008

    Article  PubMed  CAS  Google Scholar 

  • Asakura A, Rudnicki MA (2002) Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp Hematol 30:1339–1345

    Article  PubMed  Google Scholar 

  • Ashjian PH, Elbarbary AS, Edmonds B, De Ugarte D, Zhu M, Zuk PA, Lorenz P, Benhaim P, Hedrick MH (2003) In vitro differentiation of human processed lipoaspirate cells into early neural progenitors. Plast Reconstr Surg 111:1922–1931

    Article  PubMed  Google Scholar 

  • Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, Jin DK, Dias S, Zhang F, Hartman TE, Hackett NR, Crystal RG, Witte L, Hicklin DJ, Bohlen P, Eaton D, Lyden D, Sauvage F de, Rafii S (2004) Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med 10:64–71

    Article  PubMed  CAS  Google Scholar 

  • Barker JN, Wagner JE (2003) Umbilical cord blood transplantation: current practice and future innovations. Crit Rev Oncol Hematol 48:35–43

    PubMed  Google Scholar 

  • Becker PS, Nilsson SK, Li Z, Berrios VM, Dooner MS, Cooper CL, Hsieh C-C, Quesenberry PJ (1999) Adhesion receptor expression by hematopoietic cell lines and murine progenitors: modulation by cytokines and cell cycle status. Exp Hematol 27:533–541

    Article  PubMed  CAS  Google Scholar 

  • Berrios VM, Dooner GJ, Nowakowski G, Frimberger A, Valinski H, Quesenberry PJ, Becker PS (2001) The molecular basis for the cytokine-induced defect in homung and engraftment of hematopoietic stem cells. Exp Hematol 29:1326–1335

    Article  PubMed  CAS  Google Scholar 

  • Bertolini F, Battaglia M, Lanza A, Gibelli N, Palermo B, Pavesi L, Caprotti M, Robustelli della Cuna G (1997) Multilineage long-term engraftment potential of drug-resistant hematopoietic progenitors. Blood 8:3027–3036

    Google Scholar 

  • Bjornsson CRR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL (1999) Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science 283:534–537

    Article  PubMed  Google Scholar 

  • Boquest AC, Shahdadfar A, Fronsdal K, Sigurjonsson O, Tunheim SH, Collas P, Brichmann JE (2005) Isolation and transcription profiling of purified uncultured human stromal stem cells. Alteration of gene expression after in vitro cell culture. Mol Biol Cell 16:1131–1141

    Article  PubMed  CAS  Google Scholar 

  • Chaudhary PM, Roninson IB (1991) Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells. Cell 66:85–94

    Article  PubMed  CAS  Google Scholar 

  • Colter DC, Sekiya I, Prockop DJ (2001) Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci USA 98:7841–7845

    Article  PubMed  CAS  Google Scholar 

  • Cortés F, Deschaseaux F, Uchida N, Labastie M-C, Friera AM, He D, Charbord P, Péault B (1999) HCA, an immunoglobulin-like adhesion molecule present on the earliest human hematopoietic precursor cells, is also expressed by stromal cells in blood-forming tissues. Blood 93:826–837

    PubMed  Google Scholar 

  • Dalmau SR, Freitas CS, Savino W (1999) Upregulated expression of fibronectin receptors underlines the adhesive capability of thymocytes to thymic epithelial cells during the early stages of differentiation: lessons from sublethally irradiated mice. Blood 93:974–990

    PubMed  CAS  Google Scholar 

  • Deschaseaux F, Gindraux F, Saadi R, Obert L, Chalmers D, Herve P (2003) Direct selection of human bone marrow mesenchymal stem cells using an anti-CD49a antibody reveals their CD45med.low phenotype. Br J Haematol 122:506–517

    Article  PubMed  Google Scholar 

  • De Ugarte DA, Alfonso Z, Zuk PA, Elbarbary A, Zhu M, Ashjian P, Benhaim P, Hedrick MH, Fraser JK (2003) Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol Lett 89:267–270

    Article  PubMed  CAS  Google Scholar 

  • Deans RJ, Moseley AB (2000) Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 28:875–884

    Article  PubMed  CAS  Google Scholar 

  • Devine SM, Bartholomew AM, Mahmud N, Patil S, Hardy W, Sturgeon C, Hewett T, Chung T, Stock W, Sher D, Weissman S, Ferrer K, Mosca J, Deans R, Moseley A, Hoffman R (2001) Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hematol 29:244–255

    Article  PubMed  CAS  Google Scholar 

  • Devine SM, Cobbs C, Jennings M, Bartholomew AM, Hoffman R (2003) Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates. Blood 101:2999–3001

    Article  PubMed  CAS  Google Scholar 

  • Dicker A, LeBlanc K, Astrom G, Van Harmelen V, Gotherstrom C, Blomqvist L, Arner P, Ryden M (2005) Functional studies of mesenchymal stem cells derived from adult human adipose tissue. Exp Cell Res 308:283–290

    Article  PubMed  CAS  Google Scholar 

  • Dorrel C, Gan OI, Pereira DS, Hawley RG, Dick JE (2000) Expansion of human cord blood CD34+CD38- cells in ex vivo culture during retroviral transduction without a corresponding increase in SCID repopulating cell (SRC) frequency: dissociation of SRC phenotype and function. Blood 95:102–110

    PubMed  Google Scholar 

  • Dragoo JL, Lieberman JR, Lee RS, De Ugarte DA, Lee Y, Zuk PA, Hedrick MH, Benhaim P (2005) Tissue engineered bone from BMP-2- transduced stem cells derived from human fat. Plast Reconstr Surg 115:1665–1673

    Article  PubMed  CAS  Google Scholar 

  • Driessen RL, Johnston HM, Nilsson SK (2003) Membrane-bound stem cell factor is a key regulator in the initial lodgment of stem cells within the endosteal marrow region. Exp Hematol 31:1284–1291

    Article  PubMed  CAS  Google Scholar 

  • Erdo F, Buhrle C, Blunk J, Hoehn M, Xia Y, Fleishmann B, Focking M, Kustermann E, Kolossov E, Hescheler J, Hossmann KA, Trapp T (2003) Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. J Cereb Blood Flow Metab 23:780–785

    Article  PubMed  Google Scholar 

  • Fernandes KJL, McKenzie IA, Mill P, Smith KM, Akhavan M, Barnabé-Heider F, Biernaskie J, Junek A, Kobayashi NR, Toma JG, Kaplan DR, Labosky PA, Rafuse V, Hui C-C, Miller FD (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6:1082–1092

    Article  PubMed  CAS  Google Scholar 

  • Fibbe WE, Noort WA (2003) Mesenchymal stem cells and hematopoietic stem cell transplantation. Ann N Y Acad Sci 996:235–244

    PubMed  Google Scholar 

  • Foguenne J, Huygen S, Greimers R, Beguin Y, Gothot A (2005) Modulation of homing properties of primitive progenitor cells generated by ex vivo expansion. Haematology 90:445–451

    CAS  Google Scholar 

  • Fortunel NO, Otu HH, Ng H-H, Chen J, Mu X, Chevassut T, Li X, Joseph M, Bailey C, Hatzfeld JA, Hatzfeld A, Usta F, Veja VB, Long PM, Libermann TA, Lim B (2003) Comment on “stemness”: transcriptional profiling of embryonic and adult stem cells and a “stem cell molecular signature”. Science 302:393b

    Article  Google Scholar 

  • Fox NE, Kaushansky K (2005) Engagement of integrin alpha4 beta1 enhances thrombopoietin-induced megakaryopoiesis. Exp Hematol 33:94–99

    Article  PubMed  CAS  Google Scholar 

  • Fraser JK (2002) Adipose tissue: challenging the marrow monopoly. Cytotherapy 4:509–510

    Article  PubMed  CAS  Google Scholar 

  • Fraser JK, Schreiber RE, Zuk PA, Hedrick MH (2004) Adult stem cell therapy for the heart. Int J Biochem Cell Biol 36:658–666

    Article  PubMed  CAS  Google Scholar 

  • Galli R, Borello U, Gritti A, Minasi MG, Bjomson C, Coletta M, Mora M, De Angelis MG, Fiocco R, Cossu G, Vescovi AL (2000) Skeletal myogenic potential of human and mouse neural stem cells. Nat Neurosci 3:986–991

    Article  PubMed  CAS  Google Scholar 

  • Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797–1806

    Article  PubMed  CAS  Google Scholar 

  • Gothot A, Giet O, Huygen S, Beguin Y (2003) Binding and migration across fibronectin and VCAM-1 of cycling hematopoietic progenitor cells. Leuk Lymphoma 44:1379–1383

    Article  PubMed  CAS  Google Scholar 

  • Groh ME, Maitra B, Szekely E, Koç OM (2005) Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Exp Hematol 33:928–934

    Article  PubMed  CAS  Google Scholar 

  • Harris RG, Herzog EL, Bruscia EM, Grove JE, VanArnam JS, Krause DS (2004) Lack of a fusion requirement for development of bone marrow-derived epithelia. Science 305:90–93

    Article  PubMed  CAS  Google Scholar 

  • Heng BC, Cao T, Haider HK, Wang DZM, Sim EK-W, Ng SC (2004) An overview and synopsis of techniques for directing stem cell differentiation in vitro. Cell Tissue Res 315:291–303

    Article  PubMed  Google Scholar 

  • Heng BC, Hong HY, Cao T (2005) Modulating gene expression in stem cells without recombinant DNA and permanent genetic modification. Cell Tissue Res 321:147–150

    Article  PubMed  CAS  Google Scholar 

  • Horwitz EM, Gordon PL, Koo WK, Neel MD, McNall RY, Muul L, Hofmann T (2002) Isolated allogenenic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell based therapy of bone. Proc Natl Acad Sci USA 99:8932–8937

    Article  PubMed  CAS  Google Scholar 

  • Howell JC, Lee W-H, Morison P, Zhong J, Yoder MC, Srour EF (2003) Pluripotent stem cells identified in multiple murine tissues. Ann N Y Acad Sci 996:158–173

    PubMed  CAS  Google Scholar 

  • Huang JI, Steven BS, Beanes SR, Zhu M, Lorenz P, Hedrick MH, Benhaim P (2002) Rat extramedullary adipose tissue as a source of osteochondrogenic progenitor cells. Plast Reconstr Surg 109:1033–1041

    Article  PubMed  Google Scholar 

  • Huang JI, Zuk PA, Jones NF, Zhu M, Lorenz HP, Hedrick MH, Benhaim P (2004) Chondrogenic potential of multipotential cells from human adipose tissue. Plast Reconst Sur 113:585–594

    Article  Google Scholar 

  • Huss R (2000) Isolation of primary and immortalized CD34-hematopoietic and mesenchymal stem cells from various sources. Stem Cells 18:1–9

    Article  PubMed  CAS  Google Scholar 

  • Int’Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, Bezooijen RL van, Beekhuizen W, Willemze R, Kanhai HH, Fibbe WE (2003a) Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematology 88:845–852

    Google Scholar 

  • Int’Anker PS, Noort WA, Kruisselbrink AB, Scherjon SA, Beekhuizen W, Willemze R, Kanhai HH, Fibbe WE (2003b) Nonexpanded primary lung and bone marrow-derived mesenchymal cells promote the engraftment of umbilical cord blood-derived CD34+ cells in NOD/SCID mice. Exp Hematol 31:881–889

    Article  PubMed  Google Scholar 

  • Jack GS, Almeida FG, Zhang R, Alfonso ZC, Zuk PA, Rodriguez LV (2005) Processed lipoaspirate cells for tissue engineering of the lower urinary tract: implications for the treatment of stress urinary incontinence and bladder reconstruction. J Urol 174:2041–2045

    Article  PubMed  CAS  Google Scholar 

  • Jahoda CAB, Whitehouse CJ, Reynolds AJ, Hole N (2003) Hair follicle dermal cells differentiate into adipogenic and osteogenic lineages. Exp Dermatol 12:849–859

    Article  PubMed  Google Scholar 

  • Jackson KA, Mi T, Goodell MA (1999) Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci USA 96:14482–14486

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41–49

    Article  PubMed  CAS  Google Scholar 

  • Kim SJ, Cho HH, Kim YJ, Seo SY, Kim HN, Lee JB, Kim JH, Chung JS, Jung JS (2005) Human adipose tissue stromal cells expanded in human serum promote engraftment of human peripheral blood hematopoietic stem cells in NOD/SCID mice. Biochem Biophys Res Comm 329:25–31

    Article  PubMed  CAS  Google Scholar 

  • Koç ON, Peters C, Aubourg P, Raghavan S, Dyhouse S, DeGasperi R, Kolodny EH, Yoseph YB, Gerson SL, Lazarus HM, Caplan AI, Watkins PA, Krivit W (1999) Bone marrow-derived mesenchymal stem cells remain host-derived despite successful hematopoietic engraftment after allogeneic transplantation in patients with lysosomal and peroxisomal storage diseases. Exp Hematol 27:1675–1681

    Article  PubMed  Google Scholar 

  • Kögler G, Sensken S, Airey JA, Trapp T, Müschen M, Feldhahn N, Liedtke S, Sorg RV, Fischer J, Rosenbaum C, Greschat S, Knipper A, Bender J, Degistirici O, Gao J, Caplan AI, Colletti EJ, Almeida-Porada G, Müller HW, Zanjani E, Wernet P (2004) A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 200:123–135

    Article  PubMed  Google Scholar 

  • Kögler G, Radtke TF, Lefort A, Sensken S, Fischer J, Song RV, Wernet P (2005) Cytokine production and hematopoiesis support activity of cord blood-derived unrestricted somatic stem cells. Exp Hematol 33:573–583

    Article  PubMed  CAS  Google Scholar 

  • Kollet O, Peled A, Petit I, Byk T, Hershkovitz R, Guetta E, Barkai G, Nagler A, Lapidot T (2001) Rapid and efficient homing of human CD34+CD38-/lowCxCr4+ stem and progenitor cells to the bone marrow and spleen of NOD/SCID and NOD/SCID/B2mnull mice. Blood 97:3283–3291

    Article  PubMed  CAS  Google Scholar 

  • Krause DS (2005) Engraftment of bone marrow-derived epithelial cells. Ann N Y Acad Sci 1044:117–124

    Article  PubMed  Google Scholar 

  • Kucia M, Ratajczak J, Ratajczak MZ (2005) Are bone marrow stem cells plastic or heterogeneous—that is the question. Exp Hematol 33:613–623

    Article  PubMed  Google Scholar 

  • Lako M, Armstrong L, Cairns PM, Haris S, Hole N, Jahoda CAB (2002) Hair follicle dermal cells repopulate the mouse haematopoietic system. J Cell Sci 115:3967–3974

    Article  PubMed  CAS  Google Scholar 

  • Lambert J-F, Liu M, Colvin GA, Dooner M, McAuliffe CI, Becker P, Forget BG, Weissman SM, Quesenberry PJ (2003) Marrow stem cells shift gene expression and engraftment phenotype with cell cycle transit. J Exp Med 197:1563–1572

    Article  PubMed  CAS  Google Scholar 

  • Lazarus HM, Haynesworth SE, Gerson SL, Calan AI (1997) Human bone marrow-derived mesenchymal (stromal), progenitor cells (MPCs) cannot be recovered from peripheral blood progenitor cell collections. J Hematother 6:447–455

    PubMed  CAS  Google Scholar 

  • Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, Wang X, Finegold M, Weissman I, Grompe M (2000) Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 6:1229–1234

    Article  PubMed  CAS  Google Scholar 

  • Levesque JB, Takamatsu Y, Hilsson SK, Haylock DN, Simmons RJ (2001) Vascular cell adhesion molecule-1 (VCAM-1) is cleaved by neutrophil proteases in the bone marrow following hematopoietic cell mobilization by granulocyte colony stimulating factor. Blood 98:1289–1299

    Article  PubMed  CAS  Google Scholar 

  • Maitra B, Szekely E, Gjini K, Laughlin MJ, Dennis J, Haymesworth SE, Koç ON (2004) Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplant 33:597–604

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Estrada OM, Munoz-Santos Y, Julve J, Reina M, Vilaro S (2005) Human adipose tissue as a source of Flk-1+ cells: new method of differentiation and expansion. Cardiovasc Res 65:328–333

    Article  PubMed  CAS  Google Scholar 

  • McKinney-Freeman S, Goodell MA (2004) Circulating hematopoietic stem cells do not efficiently home to bone marrow during homeostasis. Exp Hematol 32:868–876

    Article  PubMed  CAS  Google Scholar 

  • McKinney-Freeman S, Jackson K, Camargo F, Ferrari G, Mavilio F, Goodell M (2002) Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Acad Sci USA 99:1341–1346

    Article  PubMed  CAS  Google Scholar 

  • Miguell JJ, Erices A, Conget P (2001) Mesenchymal stem cells. Exp Biol Med 226:507–520

    Google Scholar 

  • Miranville A, Heeschen C, Sengenes C, Curat AC, Busse R, Bouloumie A (2004) Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 110:349–355

    Article  PubMed  CAS  Google Scholar 

  • Mizuno H, Zuk PA, Zhu M, Lorenz HP, Benhaim P, Hedrick MH (2002) Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr Surg 109:199–209

    Article  PubMed  Google Scholar 

  • Morris RJ, Liu Y, Yang L, Trempus C, Li S, Lin JS, Sawicki JA, Cotsarelis G (2004) Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 22:411–417

    Article  PubMed  CAS  Google Scholar 

  • Noort WA, Kruisselbrink AB, Int’Anker PS, Kruger M, Bezooijen RL van, Paus RA de, Heemskerk MH, Lowik CW, Willemza R, Fibbe WE (2002) Mesenchymal stem cells promote engraftment of human umbilical cord blood-derived CD34+ cells in NOD/SCID mice. Exp Hematol 30:870–878

    Article  PubMed  Google Scholar 

  • Planat-Bénard V, Menard C, André M, Puceat M, Perez A, Garcia-Verdugo J-M, Pénicaud L, Casteilla L (2004) Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ Res 94:223–229

    Article  PubMed  CAS  Google Scholar 

  • Poliakova L, Pirone A, Farese A, MavVittie T, Farney A (2004) Presence of nonhematopoietic side population cells in the adult human and nonhuman primate pancreas. Transplant Proc 36:1166–1168

    Article  PubMed  CAS  Google Scholar 

  • Quesenberry PJ, Colvin GA, Lambert JF (2002) The chiaroscuro stem cell: a unified stem cell theory. Blood 100:4266–4271

    Article  PubMed  CAS  Google Scholar 

  • Quesenberry PJ, Colvin G, Lambert JF, Abedi M, Cerny J, Dooner M, Moore B, McAuliffe C, Demers D, Greer D, Parent A, Badiavas E, Lum L, Falanga V (2003) Marrow stem cell potential within a continuum. Ann N Y Acad Sci 996:209–221

    PubMed  CAS  Google Scholar 

  • Quesenberry PJ, Dooner G, Colvin G, Abedi M (2005a) Stem cell biology and the plasticity polemic. Exp Hematol 33:389–394

    Article  PubMed  CAS  Google Scholar 

  • Quesenberry PJ, Colvin G, Abedi M (2005b) Perspective: fundamental and clinical concepts on stem cell homing and engraftment: a journey to niches and beyond. Exp Hematol 33:9–19

    Article  PubMed  Google Scholar 

  • Rangappa S, Fen C, Lee EH, Bongso A, Wei ES (2003) Transformation of adult mesenchymal stem cells isolated from the fatty tissue into cardiomyocytes. Ann Thorac Surg 75:775–779

    Article  PubMed  Google Scholar 

  • Reyes M, Lund T, Lenvik T, Aguiar D, Koodie L, Verfaillie CM (2001) Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98:2615–2625

    Article  PubMed  CAS  Google Scholar 

  • Rieger K, Marinets O, Fietz T, Körper S, Sommer D, Mücke C, Reufi B, Blau WI, Thiel E, Knauf WU (2005) Mesenchymal stem cells remain of host origin even a long time after allogeneic peripheral blood stem cell or bone marrow transplantation. Exp Hematol 33:605–611

    Article  PubMed  CAS  Google Scholar 

  • Rovó A, Meyer-Monard S, Heim D, Arber C, Passweg JR, Gratwohl A, Tichelli A (2005) No evidence of plasticity in hair follicles of recipients after allogeneic hematopoietic stem cell transplantation. Exp Hematol 33:909–911

    Article  PubMed  CAS  Google Scholar 

  • Roy V, Verfaillie CM (1999) Expression and function of cell adhesion molecules on fetal liver, cord blood and bone marrow hematopoietic progenitors: implications for anatomical localization and developmental stage specific regulation of hematopoiesis. Exp Hematol 27:302–312

    Article  PubMed  CAS  Google Scholar 

  • Sackstein R (2004) The bone marrow is akin to skin: HCELL and the biology of hematopoietic stem cell homing. J Invest Dermatol 122:1061–1069

    Article  PubMed  CAS  Google Scholar 

  • Satoh H, Kishi K, Tanaka T, Kubota Y, Nakajima T, Akasaka Y, Ishii T (2004) Transplanted mesenchymal stem cells are effective for skin regeneration in acute cutaneous wounds. Cell Transplant 13:405–412

    PubMed  Google Scholar 

  • Shi C, Mai Y, Cheng T (2004) Identification of hematopoietic cell populations from the dermal papillae of human hair follicles. Transpl Proc 36:3206–3211

    Google Scholar 

  • Shih DT, Lee DC, Chen SC, Tsai RY, Huang CT, Tsai CC, Shen EY, Chiu WT (2005) Isolation and characterization of neurogenic mesenchymal stem cells in human scalp tissue. Stem Cells 23:1012–1020

    Article  PubMed  CAS  Google Scholar 

  • Shibayama H, Anzai N, Ritchie A, Zhang S, Mantel C, Broxmeyer HE (1998) Interleukin-3 and Flt3-ligand induce adhesion of Baf3/Flt3 precursor B-lymphoid cells to fibronectin via activation of VLA-4 and VLA-5. Cell Immunol 187:27–33

    Article  PubMed  CAS  Google Scholar 

  • Solanilla A, Grosset C, Duchez P, Legembre P, Pitard V, Dupouy M, Belloc F, Viallard JF, Reiffers J, Boiron JM, Coulombet L, Ripoche J (2003) Flt3-ligand induces adhesion of haematopoietic progenitor cells via a very late antigen (VLA)-4 and VLA-5-dependent mechanism. Br J Haematol 120:782–786

    Article  PubMed  CAS  Google Scholar 

  • Thalmeier K, Meissner P, Moosmann S, Sagebiel S, Wiest I, Huss R (2001) Mesenchymal differentiation and organ distribution of established human stromal cell lines in NOD/SCID mice. Acta Haematol 105:159–165

    Article  PubMed  CAS  Google Scholar 

  • Toma JG, Akhavan M, Fernandes KJL, Barnabé-Heider F, Sadikot A, Kaplan DR, Miller FD (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3:778–784

    Article  PubMed  CAS  Google Scholar 

  • Vassilopoulos G, Wang P-R, Russel DW (2003) Transplanted bone marrow regenerates liver by cell fusion. Nature 422:901–903

    Article  PubMed  CAS  Google Scholar 

  • Verfaillie CM, Schwartz R, Reyes M, Jiang Y (2003) Unexpected potential of adult stem cells. Ann N Y Acad Sci 996:231–233

    Article  PubMed  CAS  Google Scholar 

  • Waller EK, Olweus J, Lund-Johansen F, Huang S, Nguyen M, Guo G-R, Terstappen L (1995) The “common stem cell” hypothesis reevaluated: human fetal bone marrow contains separate populations of hematopoietic and stromal progenitors. Blood 9:2422–2435

    Google Scholar 

  • Wang X, Al-Dhalimy M, Lagasse E, Finegold M, Grompe M (2002) Kinetics of liver repopulation after bone marrow transplantation. Am J Pathol 161:565–574

    PubMed  Google Scholar 

  • Wang X, Willenbring H, Akkari Y, Torimaru Y, Foster M, Al-Dhalimy M, Lagasse E, Finegold M, Olson S, Grompe M (2003) Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422:897–900

    Article  PubMed  CAS  Google Scholar 

  • Wright D, Wagers A, Gulati A, Johnson F, Weissman I (2001) Physiological migration of hematopoietic stem and progenitor cells. Science 294:1933–1936

    Article  PubMed  CAS  Google Scholar 

  • Yanai N, Obinata M (2001) Oncostatin M regulates mesenchymal cell differentiation and enhances hematopoietic supportive activity of bone marrow stromal cell lines. In Vitro Cell Dev Biol Anim 37:698–704

    Article  PubMed  CAS  Google Scholar 

  • Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tiss Engineer 7:211–228

    Article  CAS  Google Scholar 

  • Zuk PA, Zhu M, Ashjian PA, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Instituto National de Cancer, Oncohematology Research Program,Centro de Pesquisa, Rua André Cavalcante 37, 6 andar, Centro, Rio de Janeiro, RJ, CEP 20230-030, Brazil

    Claudia Sondermann Freitas

  2. IBRAG, Department of Biochemistry, Rio de Janeiro State University, Rio de Janeiro, 22471-030, Brazil

    Sergio Ranto Dalmau

  3. Instituto Nacional de Cancer, Pesquisa, Rua André Cavalcante 37-60 Andar, Centro, Rio de Janeiro,, RJ, CEP20230-030, Brazil

    Claudia Sondermann Freitas

Authors
  1. Claudia Sondermann Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sergio Ranto Dalmau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudia Sondermann Freitas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Freitas, C.S., Dalmau, S.R. Multiple sources of non-embryonic multipotent stem cells: processed lipoaspirates and dermis as promising alternatives to bone-marrow-derived cell therapies. Cell Tissue Res 325, 403–411 (2006). https://doi.org/10.1007/s00441-006-0172-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-006-0172-x

Keywords

Search

Navigation