Critical Variables in the Conversion of Marrow Cells to Skeletal Muscle

Overview

Journal Blood

Publisher Elsevier

Specialty Hematology

Date 2005 May 5

PMID 15870176

Citations 5

Authors

Mehrdad Abedi

Deborah A Greer

Bethany M Foster

Gerald A Colvin

Joshua A Harpel

Delia A Demers

Jeffery Pimentel

Mark S Dooner

Peter J Quesenberry

Affiliations

Soon will be listed here.

Abstract

We have studied conversion of marrow cells to skeletal muscle in cardiotoxin-injured anterior tibialis muscle in a green fluorescent protein (GFP) to C57BL/6 transplantation model and ascertained that total body irradiation (TBI) with establishment of chimerism is a critical factor. Local irradiation has little effect in lower doses and was detrimental at higher doses. Whole body (1000 cGy) with shielding of the leg or a combination of 500 cGy TBI and 500 cGy local radiations was found to give the best results. In non-obese diabetic-severe combined immunodeficient (NOD-SCID) recipients, we were able to show that conversion could occur without radiation, albeit at relatively lower levels. Within 3 days of cardiotoxin injury, GFP-positive mononuclear cells were seen in the muscle, and within 2 weeks GFP-positive muscle fibers were identified. Conversion rates were increased by increasing donor-cell dose. Timing of the cardiotoxin injury relative to the transplantation was critical. These studies show that variables in transplantation and injury are critical features of marrow-to-muscle conversions. Irradiation primarily effects conversion by promoting chimerism. These data may explain the differences in the literature for the frequency of marrow-to-skeletal muscle conversion and can set a platform for future models and perhaps clinical protocols.

Citing Articles

Epigenetic regulation of embryonic ectoderm development in stem cell differentiation and transformation during ontogenesis.

Huang L, Li F, Ye L, Yu F, Wang C Cell Prolif. 2023; 56(4):e13413.

PMID: 36727213 PMC: 10068960. DOI: 10.1111/cpr.13413.

Marrow Hematopoietic Stem Cells Revisited: They Exist in a Continuum and are Not Defined by Standard Purification Approaches; Then There are the Microvesicles.

Quesenberry P, Goldberg L, Aliotta J, Dooner M Front Oncol. 2014; 4:56.

PMID: 24772390 PMC: 3983521. DOI: 10.3389/fonc.2014.00056.

Bone marrow-derived stromal cells are invasive and hyperproliferative and alter transforming growth factor-α-induced pulmonary fibrosis.

Madala S, Edukulla R, Schmidt S, Davidson C, Ikegami M, Hardie W Am J Respir Cell Mol Biol. 2013; 50(4):777-86.

PMID: 24199692 PMC: 4068918. DOI: 10.1165/rcmb.2013-0042OC.

Induction and survival of binucleated Purkinje neurons by selective damage and aging.

Magrassi L, Grimaldi P, Ibatici A, Corselli M, Ciardelli L, Castello S J Neurosci. 2007; 27(37):9885-92.

PMID: 17855603 PMC: 6672639. DOI: 10.1523/JNEUROSCI.2539-07.2007.

Alteration of marrow cell gene expression, protein production, and engraftment into lung by lung-derived microvesicles: a novel mechanism for phenotype modulation.

Aliotta J, Sanchez-Guijo F, Dooner G, Johnson K, Dooner M, Greer K Stem Cells. 2007; 25(9):2245-56.

PMID: 17556595 PMC: 3376082. DOI: 10.1634/stemcells.2007-0128.

References

Peichev M, Naiyer A, Pereira D, Zhu Z, Lane W, Williams M . Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood. 2000; 95(3):952-8. View

Fukada S, Miyagoe-Suzuki Y, Tsukihara H, Yuasa K, Higuchi S, Ono S . Muscle regeneration by reconstitution with bone marrow or fetal liver cells from green fluorescent protein-gene transgenic mice. J Cell Sci. 2002; 115(Pt 6):1285-93. DOI: 10.1242/jcs.115.6.1285. View

Wells D, Wells K, Asante E, Turner G, Sunada Y, Campbell K . Expression of human full-length and minidystrophin in transgenic mdx mice: implications for gene therapy of Duchenne muscular dystrophy. Hum Mol Genet. 1995; 4(8):1245-50. DOI: 10.1093/hmg/4.8.1245. View

Camargo F, Green R, Capetanaki Y, Jackson K, Goodell M, Capetenaki Y . Single hematopoietic stem cells generate skeletal muscle through myeloid intermediates. Nat Med. 2003; 9(12):1520-7. DOI: 10.1038/nm963. View

Wang X, Montini E, Al-Dhalimy M, Lagasse E, Finegold M, Grompe M . Kinetics of liver repopulation after bone marrow transplantation. Am J Pathol. 2002; 161(2):565-74. PMC: 1850741. DOI: 10.1016/S0002-9440(10)64212-5. View

Bittner R, Schofer C, Weipoltshammer K, Ivanova S, Streubel B, Hauser E . Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice. Anat Embryol (Berl). 1999; 199(5):391-6. DOI: 10.1007/s004290050237. View

Phelps S, Hauser M, COLE N, Rafael J, Hinkle R, Faulkner J . Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum Mol Genet. 1995; 4(8):1251-8. DOI: 10.1093/hmg/4.8.1251. View

Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M . Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999; 85(3):221-8. DOI: 10.1161/01.res.85.3.221. View

Steinbauer M, Guba M, Cernaianu G, Kohl G, Cetto M, Kunz-Schughart L . GFP-transfected tumor cells are useful in examining early metastasis in vivo, but immune reaction precludes long-term tumor development studies in immunocompetent mice. Clin Exp Metastasis. 2003; 20(2):135-41. DOI: 10.1023/a:1022618909921. View

10.

Badiavas E, Abedi M, Butmarc J, Falanga V, Quesenberry P . Participation of bone marrow derived cells in cutaneous wound healing. J Cell Physiol. 2003; 196(2):245-50. DOI: 10.1002/jcp.10260. View

11.

Pereira R, Halford K, OHara M, Leeper D, Sokolov B, Pollard M . Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci U S A. 1995; 92(11):4857-61. PMC: 41806. DOI: 10.1073/pnas.92.11.4857. View

12.

Ferrari G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F . Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 1998; 279(5356):1528-30. DOI: 10.1126/science.279.5356.1528. View

13.

Lagasse E, CONNORS H, Reitsma M, Dohse M, Osborne L, Wang X . Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med. 2000; 6(11):1229-34. DOI: 10.1038/81326. View

14.

Theise N, Badve S, Saxena R, Henegariu O, Sell S, Crawford J . Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology. 1999; 31(1):235-40. DOI: 10.1002/hep.510310135. View

15.

Kotton D, Ma B, Cardoso W, Sanderson E, Summer R, Williams M . Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development. 2001; 128(24):5181-8. DOI: 10.1242/dev.128.24.5181. View

16.

Cuzick J . A Wilcoxon-type test for trend. Stat Med. 1985; 4(1):87-90. DOI: 10.1002/sim.4780040112. View

17.

Abedi M, Greer D, Colvin G, Demers D, Dooner M, Harpel J . Robust conversion of marrow cells to skeletal muscle with formation of marrow-derived muscle cell colonies: a multifactorial process. Exp Hematol. 2004; 32(5):426-34. DOI: 10.1016/j.exphem.2004.02.007. View

18.

Rosenzweig M, Connole M, Glickman R, Yue S, NOREN B, Demaria M . Induction of cytotoxic T lymphocyte and antibody responses to enhanced green fluorescent protein following transplantation of transduced CD34(+) hematopoietic cells. Blood. 2001; 97(7):1951-9. DOI: 10.1182/blood.v97.7.1951. View

19.

LaBarge M, Blau H . Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell. 2002; 111(4):589-601. DOI: 10.1016/s0092-8674(02)01078-4. View

20.

Wakitani S, Saito T, Caplan A . Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve. 1995; 18(12):1417-26. DOI: 10.1002/mus.880181212. View