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Existence of Reserve Quiescent Stem Cells in Adults, From Amphibians to Humans

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Regeneration: Stem Cells and Beyond

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 280))

Abstract

Several theories have been proposed to explain the phenomenon of tissue restoration in amphibians and higher order animals. These theories include dedifferentiation of damaged tissues, transdifferentiation of lineage-committed stem cells, and activation of quiescent stem cells. Young and colleagues demonstrated that connective tissues throughout the body contain multiple populations of quiescent lineagecommitted progenitor stem cells and lineage-uncommitted pluripotent stem cells. Subsequent cloning and cell sorting studies identified quiescent lineage-uncommitted pluripotent mesenchymal stem cells, capable of forming any mesodermal cell type, and pluripotent epiblastic-like stem cells, capable of forming any somatic cell type. Based on their studies, they propose at least 11 categories of quiescent reserve stem cells resident within postnatal animals, including humans. These categories are pluripotent epiblastic-like stem cells, pluripotent ectodermal stem cells, pluripotent epidermal stem cells, pluripotent neuronal stem cells, pluripotent neural crest stem cells, pluripotent mesenchymal (mesodermal) stem cells, pluripotent endodermal stem cells, multipotent progenitor stem cells, tripotent progenitor stem cells, bipotent progenitor stem cells, and unipotent progenitor stem cells. Thus, activation of quiescent reserve stem cells, i.e., lineage-committed progenitor stem cells and lineage-uncommitted pluripotent stem cells, resident within the connective tissues could provide for the continual maintenance and repair of the postnatal organism after birth.

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References

  • Ailhaud G, Grimaldi P, Negrel R (1992) Cellular and molecular aspects of adipose tissue development. Annu Rev Nutr 12:207–33

    Article  PubMed  CAS  Google Scholar 

  • Beresford JN (1989) Osteogenic stem cells and the stromal system of bone and marrow. Clin Orthop 240:270–80

    PubMed  Google Scholar 

  • Bjornson CR, 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  CAS  Google Scholar 

  • Campion, DR (1984) The muscle satellite cell: a review. Int Rev Cytol 87:225–251

    Article  PubMed  CAS  Google Scholar 

  • Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9:641–650

    Article  PubMed  CAS  Google Scholar 

  • Caplan AI, Elyaderani M, Mochizuki Y, Wakitani S, Goldberg V (1997) Principles of cartilage repair and regeneration. Clin Orthop Rel Res 342:254–269

    Article  Google Scholar 

  • Clarke DL, Johansson CB, Wilbertz J, Veress B, Nilsson E, Karlstrom H, Lendahl U, Frisen J (2000) Generalized potential of adult neural stem cells. Science 288:1660–1663

    Article  PubMed  CAS  Google Scholar 

  • Cruess, RL (1982) The Musculoskeletal system: embryology, biochemistry, and physiology. New York, Churchill Livingston, pp. 1–33, 109–169, 255–287

    Google Scholar 

  • Dixon K, Murphy RW, Southerland SS, Young HE, Dalton ML, Lucas PA (1996) Recombinant human bone morphogenetic proteins-2 and 4 (rhBMP-2 and rhBMP-4) induce several mesenchymal phenotypes in culture. Wound Rep Reg 4:374–380

    Article  CAS  Google Scholar 

  • Donovan PJ, Gearhart J (2001) The end of the beginning for pluripotent stem cells. Nature 414:92–927

    Article  PubMed  CAS  Google Scholar 

  • Eglitis MA, Mezey E (1997) Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci USA 94:4080–4085

    Article  PubMed  CAS  Google Scholar 

  • Farber J (1959) An experimental analysis of regional organization in the regenerating forelimb of the axolotl (Ambystoma mexicanum). Arch Biol 71:1–72

    Google Scholar 

  • Grounds MD, Garrett KL, Lai MC, Wright WE, Beilharz MW (1992) Identification of muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tiss Res 267:99–104

    Article  CAS  Google Scholar 

  • Hayflick L (1965) The limited in vitro lifetime of human diploid cell strains. Exper Cell Res 37:614–636

    Article  CAS  Google Scholar 

  • Iten LE, Bryant SV (1973) Forelimb regeneration from different levels of amputation in the newt. Notophthalamus viridescens. Length, rate, stage. Wilhelm Roux Archiv 173:77–89

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto T, Kikutani H, Borne AEGKrvd, Goyert SM, Mason D, Miyasaka M, Moretta L, Okumura K, Shaw S, Springer T, Sugamura K, Zola H (1997) Leucocyte Typing VI, White Cell Differentiation Antigens. Garland Publishing, Hamden, CT

    Google Scholar 

  • Lucas PA, Calcutt AF, Ossi P, Young HE, Southerland SS (1993) Mesenchymal stem cells from granulation tissue. J Cell Biochem 17E:122

    Google Scholar 

  • Lucas PA, Calcutt AF, Southerland SS, Wilson JA, Harvey RL, Warejcka D, Young HE (1995) A population of cells resident within embryonic and newborn rat skeletal muscle is capable of differentiating into multiple mesodermal phenotypes. Wound Rep Reg 3:457–468

    Article  Google Scholar 

  • Lucas PA, Warejcka DJ, Zhang L-M, Newman WH, Young HE (1996a) Effect of rat mesenchymal stem cells on the development of abdominal adhesions after surgery. J Surg Res 62:229–232

    Article  PubMed  CAS  Google Scholar 

  • Lucas PA, Warejcka DJ, Young HE, Lee BY (1996b) Formation of abdominal adhesions is inhibited by antibodies to transforming growth factor-betal. J Surg Res 65:135–138

    Article  PubMed  CAS  Google Scholar 

  • Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–498

    Article  PubMed  CAS  Google Scholar 

  • McGuire, WP (1998) High-dose chemotherapy and autologous bone marrow or stem cell reconstitution for solid tumors. Curr Probl Cancer 22:135–137

    Article  PubMed  CAS  Google Scholar 

  • McKinney-Freeman SL, Jackson KA, Camargo FD, Ferrari G, Mavillio F, Goodell MA (2002) Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Acad Sci USA 99:1341–1346

    Article  PubMed  CAS  Google Scholar 

  • Owen M (1988) Marrow stromal cells. J Cell Sci Suppl 10:63–76

    PubMed  CAS  Google Scholar 

  • Palis J, Segel GB (1998) Developmental biology of erythropoiesis. Blood Rev 12:1061–1064

    Article  Google Scholar 

  • Pate DW, Southerland SS, Grande DA, Young HE, Lucas PA (1993) Isolation and differentiation of mesenchymal stem cells from rabbit muscle. Surg Forum XLIV:587–589

    Google Scholar 

  • Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP (1999) Bone marrow as a potential source of hepatic oval cells. Science 284:1168–1170

    Article  PubMed  CAS  Google Scholar 

  • 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 148:143–147

    Article  Google Scholar 

  • Pritchette WH, Dent JN (1972) The role of size in the rate of limb regeneration in the adult newt. Growth 36:275–289

    Google Scholar 

  • Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74

    Article  PubMed  CAS  Google Scholar 

  • Ratajczak MZ, Pletcher CH, Mariiez W, Machlinski B, Moore J, Wasik M, Ratajczak J, Gewirtz AM (1998) CD34+, kit+, rhodamine 123 (low) phenotype identifies a marrow cell population highly enriched for human hematopoietic stem cells. Leukemia 12:942–950

    Article  PubMed  CAS  Google Scholar 

  • Rogers JJ, Young HE, Adkison LR, Lucas PA, Black AC Jr (1995) Differentiation factors induce expression of muscle, fat, cartilage, and bone in a clone of mouse pluripotent mesenchymal stem cells. Amer Surg 61:231–236

    CAS  Google Scholar 

  • Saito T, Dennis JE, Lennon DP, Young RG, Caplan AI (1995) Myogenic expression of mesenchymal stem cells within myotubes of max mice in vitro and in vivo. Tiss Eng 1:327–343

    Article  CAS  Google Scholar 

  • Scadding SR (1977) Phylogenetic distribution of limb regeneration capacity in adult amphibia. J Exp Zool 202:57–68

    Article  Google Scholar 

  • Shamblott MJ, Axelman J, Wang S, Bugg EM, Littlefield JW, Donovan PJ, Blumenthal PD, Huggins GR, Gearhart JD (1998) Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci USA 95:13726–13731

    Article  PubMed  CAS  Google Scholar 

  • Singer M (1951) Induction of regeneration of the forelimb of the frog by augmentation of the nerve supply. Proc Soc Exp Biol Med 76:413–416

    PubMed  CAS  Google Scholar 

  • Singer M (1978) On the nature of the neurotrophic phenomenon in urodele regeneration. Am Zool 18:829–841

    CAS  Google Scholar 

  • Stocum DL (1979) Stages of forelimb regeneration in Ambystoma maculatum. J ExP Zool 209:395–416

    Article  PubMed  CAS  Google Scholar 

  • Stocum DL (1998) Regenerative biology and engineering: strategies for tissue restoration. Wound Rep Reg 6:276–290

    Article  CAS  Google Scholar 

  • Tank PW, Carlson BM, Connelly TG (1976) A staging system for forelimb regeneration in the axolotl, Ambystoma mexicanum. J Morph 150:117–128

    Article  PubMed  CAS  Google Scholar 

  • Tank PW, Holder N (1981) Pattern regulation in the regenerating limbs of urodele amphibians. Quart Rev Biol 56:113–142.

    Article  Google Scholar 

  • Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147

    Article  PubMed  CAS  Google Scholar 

  • Thornton CS (1968) Amphibian limb regeneration. In: Brachet J, King TJV (eds) Advances in Morphogenesis, Academic Press, New York, Vol. 7, pp. 205–249

    Google Scholar 

  • Toole BP, Gross J (1971) The extracellular matrix of the regenerating newt limb: synthesis and removal of hyaluronate prior to differentiation. Dev Biol 25:57–77

    Article  PubMed  CAS  Google Scholar 

  • Vierck JL, McNamara JP, Dodson MV (1996) Proliferation and differentiation of progeny of ovine unilocular fat cells (adipofibroblasts). In Vitro Cell Dev Biol Anim 32:564–572

    Article  PubMed  CAS  Google Scholar 

  • Vescovi AL, Galli R, Gritti A (2001) The neural stem cells and their transdifferentiation capacity. Biomed Pharmacother 55:201–205

    Article  PubMed  CAS  Google Scholar 

  • Warejcka DJ, Harvey R, Taylor BJ, Young HE, Lucas PA (1996) A population of cells isolated from rat heart capable of differentiating into several mesodermal phenotypes. J Surg Res 62:233–242

    Article  PubMed  CAS  Google Scholar 

  • Woodbury D, Schwarz EJ, Prockop DJ, Black IB (2000) Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 61:364–370

    Article  PubMed  CAS  Google Scholar 

  • Young HE (1977a) Epidermal ridge formation during limb regeneration in the adult salamander, Ambystoma annulatum. Proc Ark Acad Sci 31:107–109

    Google Scholar 

  • Young HE (1977b) Limb regeneration in the adult salamander, Ambystoma annulatum Cope 1889 (Amphibia: Ambystomatidae). Univ. Arkansas Library Press, Fayetteville

    Google Scholar 

  • Young HE (1977c) Anomalies during limb regeneration in the adult salamander, Ambystoma annulatum. Proc Ark Acad Sci 31:110–111

    Google Scholar 

  • Young HE (1983) A Temporal Examination of Glycoconjugates During the Initiation Phase of Limb Regeneration in Adult Ambystoma. Texas Tech Univ. Library Press, Lubbock

    Google Scholar 

  • Young HE (2000) Stem cells and tissue engineering. In: Huard J, Fu FH (eds) Gene Therapy in Orthopaedic and Sports Medicine, Springer-Verlag New York, Inc., New York, NY, pp. 143–173

    Chapter  Google Scholar 

  • Young HE, Bailey CF, Dalley BK (1983a) Environmental conditions prerequisite for complete limb regeneration in the postmetamorphic adult land-phase salamander, Ambystoma. Anat Rec 206:289–294

    Article  PubMed  CAS  Google Scholar 

  • Young HE, Bailey CF, Dalley BK (1983b) Gross morphological analysis of limb regeneration in postmetamorphic adult Ambystoma. Anat Rec 206:295–306

    Article  PubMed  CAS  Google Scholar 

  • Young HE, Dalley BK, Markwald RR (1983c) Identification of hyaluronate within peripheral nervous tissue matrices during limb regeneration. In: Coates PW, Markwald RR, Kenny AD (eds), Developing and Regenerating Vertebrate Nervous Systems, Neurology and Neurobiology, Alan R. Liss, Inc., New York, 6:175–183

    Google Scholar 

  • Young HE, Bailey CF, Markwald RR, Dalley BK (1985) Histological analysis of limb regeneration in postmetamorphic adult Ambystoma. Anat Rec 212:183–194

    Article  PubMed  CAS  Google Scholar 

  • Young HE, Dalley BK, Markwald RR (1989a) Glycoconjugates in normal wound tissue matrices during the initiation phase of limb regeneration in adult Ambystoma. Anat Rec 223:223–230

    Article  PubMed  CAS  Google Scholar 

  • Young HE, Dalley BK, Markwald RR (1989b) Effect of selected denervations on glycoconjugate composition and tissue morphology during the initiation phase of limb regeneration in adult Ambystoma. Anat Rec 223:231–241

    Article  PubMed  CAS  Google Scholar 

  • Young HE, Morrison DC, Martin JD, Lucas PA (1991) Cryopreservation of embryonic chick myogenic lineage-committed stem cells. J Tiss Cult Meth 13:275–284

    Article  Google Scholar 

  • Young HE, Ceballos EM, Smith JC, Lucas PA, Morrison DC (1992a) Isolation of embryonic chick myosatellite and pluripotent mesenchymal stem cells. J Tiss Cult Meth 14:85–92

    Article  Google Scholar 

  • Young HE, Sippel J, Putnam LS, Lucas PA, Morrison DC (1992b) Enzyme-linked immuno-culture assay. J Tiss Cult Meth 14:31–36

    Article  Google Scholar 

  • Young HE, Ceballos EM, Smith JC, Mancini ML, Wright RP, Ragan BL, Bushell I, Lucas PA (1993) Pluripotent mesenchymal stem cells reside within avian connective tissue matrices. In Vitro Cell Dev Biol Anim 29A:723–736

    Article  PubMed  CAS  Google Scholar 

  • Young HE, Mancini ML, Wright RP, Smith JC, Black AC Jr, Reagan CR, Lucas PA (1995) Mesenchymal stem cells reside within the connective tissues of many organs. Dev Dynam 202:137–144

    Article  CAS  Google Scholar 

  • Young HE, Wright RP, Mancini ML, Lucas PA, Reagan CR, Black ACJr (1998a) Bioactive factors affect proliferation and phenotypic expression in pluripotent and progenitor mesenchymal stem cells. Wound Rep Reg 6:65–75

    Article  Google Scholar 

  • Young HE, Rogers JJ, Adkison LR, Lucas PA, Black ACJr (1998b) Muscle morphogenetic protein induces myogenic gene expression in Swiss-3T3 cells. Wound Rep Reg 6:530–541

    Google Scholar 

  • Young HE, Steele TA, Bray RA, Detmer K, Blake LW, Lucas PA, Black AC Jr (1999) Human pluripotent and progenitor cells display cell surface cluster differentiation markers CD10, CD13, CD56, and MHC Class-I. Proc Soc Exp Biol Med 221:63–71

    Article  PubMed  CAS  Google Scholar 

  • Young HE, Duplaa C, Young TM, Floyd JA, Reeves ML, Davis KH, Mancini GJ, Eaton ME, Hill JD, Thomas K, Austin T, Edwards C, Cuzzourt J, Parikh A, Groom J, Hudson J, Black AC Jr. (2001a) Clonogenic analysis reveals reserve stem cells in postnatal mammals. I. Pluripotent mesenchymal stem cells. Anat Rec 263:350–360

    Article  PubMed  CAS  Google Scholar 

  • Young HE, Steele T, Bray RA, Hudson J, Floyd JA, Hawkins K, Thomas K, Austin T, Edwards C, Cuzzourt J, Duenzl M, Lucas PA, Black AC Jr. (2001b) 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 264:51–62

    Article  PubMed  CAS  Google Scholar 

  • Young HE, Black Jr AC (2003) Adult stem cells. Anat Rec (in press)

    Google Scholar 

  • Young HE, Duplaa C, Romero-Ramos M, Chesselet M-F, Vourc'h P, Yost MJ, Ericson K, Terracio L, Asahara T, Masuda H, Tamura-Ninomiya S, Detmer K, Bray RA, Steele TA, Hixson D, El-Kalay M, Tobin BW, Russ RD, Horst MN, Floyd JA, Henson NL, Hawkins KC, Groom J, Blake L, Bland LJ, Thompson AJ, Kirincich A, Moreau C, Hudson J, Bowyer III FP, Lin TJ, Black Jr AC (2003a) Tissue engineering using adult reserve pluripotent stem cells. J Cell Biochem Biophys (in press)

    Google Scholar 

  • Young HE, Duplaa C, Yost MJ, Henson NL, Floyd JA, Detmer K, Thompson AJ, Powell SW, Gamblin TC, Kizziah K, Holland BJ, Boev A, Van de Water JM, Godbee DC, Edwards CR, Wu E, Cawley C, Edwards PD, Macgregor A, Bozof R, Thompson TM, Petro Jr GJ, Shelton HM, McCampbell BL, Mills JC, Flynt FL, Steele TA, Kearney M, Kirincich-Greathead A, Hardy W, Young PR, Amin AV, Williams RS, Horton MM, McGuinn S, Ericson K, Terracio L, Moreau C, Hixson D, Tobin BW, Hudson J, Bowyer III FP, Black Jr AC. (2003b) Clonogenic analysis reveals reserve stem cells in postnatal mammals. II. Pluripotent epiblastic-like stem cells. Anat Rec (submitted)

    Google Scholar 

  • Young HE, Bray RA, Detmer K, Yoder MC, Henson NL, Floyd JA, Hawkins KC, Groom J, Duenzl M, Thompson AJ, Hixson D, Hudson J, BowyerIII FP, Lin TJ, Black ACJr. (2003c) Reserve pluripotent stem cells resembling embryonic stem cells are present in adult humans. Anat Rec (submitted).

    Google Scholar 

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Young, H.E. (2004). Existence of Reserve Quiescent Stem Cells in Adults, From Amphibians to Humans. In: Heber-Katz, E. (eds) Regeneration: Stem Cells and Beyond. Current Topics in Microbiology and Immunology, vol 280. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-18846-6_2

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  • DOI: https://doi.org/10.1007/978-3-642-18846-6_2

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