Adipose stromal cells differentiate along a smooth muscle lineage pathway upon endothelial cell contact via induction of activin A

Circulation Research

Volumn 115, Issue 9, 2014, Pages 800-809

  Merfeld Clauss, Stephanie ^a,b   Lupov, Ivan P ^a,b   Lu, Hongyan ^a,b   Feng, Dongni ^a,b   Compton Craig, Peter ^a,b   March, Keith L ^a,b   Traktuev, Dmitry O ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Activin A; Adipose tissue; Coculture techniques; Endothelial cells; Mesenchymal stem cells; Neovascularization; Smooth muscle

Indexed keywords

ACTIVIN A; ALPHA SMOOTH MUSCLE ACTIN; CALPONIN; CELL ANTIGEN; FOLLISTATIN; IMMUNOGLOBULIN G; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TRANSGELIN; ACTA2 PROTEIN, HUMAN; ACTIN; ACTIN BINDING PROTEIN; ACTIVIN; ACTIVIN RECEPTOR 1; ACVR1B PROTEIN, HUMAN; ACVR1C PROTEIN, HUMAN; CALCIUM BINDING PROTEIN; FST PROTEIN, HUMAN; MUSCLE PROTEIN; PROTEIN SERINE THREONINE KINASE; SMAD2 PROTEIN, HUMAN; TGF-BETA TYPE I RECEPTOR; TGFB1 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ADIPOSE STROMAL CELL; ADIPOSE TISSUE CELL; ARTICLE; CELL CONTACT; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; COCULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MONOCULTURE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SMOOTH MUSCLE FIBER; STROMA CELL; UPREGULATION; ADIPOSE TISSUE; ANGIOGENESIS; CELL COMMUNICATION; CELL CULTURE; CELL LINEAGE; CELL MOTION; CYTOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIME;

ACTINS; ACTIVIN RECEPTORS, TYPE I; ACTIVINS; ADIPOSE TISSUE; CALCIUM-BINDING PROTEINS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; FOLLISTATIN; HUMANS; MESENCHYMAL STROMAL CELLS; MICROFILAMENT PROTEINS; MUSCLE PROTEINS; MYOCYTES, SMOOTH MUSCLE; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION;

EID: 84921981261     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.304026     Document Type: Article

References (39)

1. Asahara T, Isner JM. Endothelial progenitor cells for vascular regeneration. J Hematother Stem Cell Res. 2002;11:171-178.
2. Barbash IM, Chouraqui P, Baron J, Feinberg MS, Etzion S, Tessone A, Miller L, Guetta E, Zipori D, Kedes LH, Kloner RA, Leor J. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation. 2003;108:863-868.
3. Duan HF, Wu CT, Wu DL, Lu Y, Liu HJ, Ha XQ, Zhang QW, Wang H, Jia XX, Wang LS. Treatment of myocardial ischemia with bone marrowderived mesenchymal stem cells overexpressing hepatocyte growth factor. Mol Ther. 2003;8:467-474.
4. Kale S, Karihaloo A, Clark PR, Kashgarian M, Krause DS, Cantley LG. Bone marrow stem cells contribute to repair of the ischemically injured renal tubule. J Clin Invest. 2003;112:42-49.
5. Kawamoto A, Tkebuchava T, Yamaguchi J, et al. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation. 2003;107:461-468.
6. Orlic D. Adult bone marrow stem cells regenerate myocardium in ischemic heart disease. Ann N Y Acad Sci. 2003;996:152-157.
7. Melero-Martin JM, De Obaldia ME, Kang SY, Khan ZA, Yuan L, Oettgen P, Bischoff J. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res. 2008;103:194-202.
8. Melero-Martin JM, Khan ZA, Picard A, Wu X, Paruchuri S, Bischoff J. In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood. 2007;109:4761-4768.
9. Traktuev DO, Prater DN, Merfeld-Clauss S, Sanjeevaiah AR, Saadatzadeh MR, Murphy M, Johnstone BH, Ingram DA, March KL. Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ Res. 2009;104:1410-1420.
10. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211-228.
11. Wang C, Yin S, Cen L, Liu Q, Liu W, Cao Y, Cui L. Differentiation of adipose-derived stem cells into contractile smooth muscle cells induced by transforming growth factor-beta1 and bone morphogenetic protein-4. Tissue Eng Part A. 2010;16:1201-1213.
12. Jeon ES, Song HY, Kim MR, Moon HJ, Bae YC, Jung JS, Kim JH. Sphingosylphosphorylcholine induces proliferation of human adipose tissue-derived mesenchymal stem cells via activation of JNK. J Lipid Res. 2006;47:653-664.
13. Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, Pell CL, Johnstone BH, Considine RV, March KL. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation. 2004;109:1292-1298.
14. Miranville A, Heeschen C, Sengenès C, Curat CA, Busse R, Bouloumié A. Improvement of postnatal neovascularization by human adipose tissuederived stem cells. Circulation. 2004;110:349-355.
15. Planat-Benard V, Silvestre JS, Cousin B, André M, Nibbelink M, Tamarat R, Clergue M, Manneville C, Saillan-Barreau C, Duriez M, Tedgui A, Levy B, Pénicaud L, Casteilla L. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation. 2004;109:656-663.
16. Cai L, Johnstone BH, Cook TG, Liang Z, Traktuev D, Cornetta K, Ingram DA, Rosen ED, March KL. Suppression of hepatocyte growth factor production impairs the ability of adipose-derived stem cells to promote ischemic tissue revascularization. Stem Cells. 2007;25:3234-3243.
17. Mazo M, Hernández S, Gavira JJ, Abizanda G, Araña M, López-Martínez T, Moreno C, Merino J, Martino-Rodríguez A, Uixeira A, García de Jalón JA, Pastrana J, Martínez-Caro D, Prósper F. Treatment of reperfused ischemia with adipose-derived stem cells in a preclinical Swine model of myocardial infarction. Cell Transplant. 2012;21:2723-2733.
18. Mazo M, Cemborain A, Gavira JJ, et al. Adipose stromal vascular fraction improves cardiac function in chronic myocardial infarction through differentiation and paracrine activity. Cell Transplant. 2012;21:1023-1037.
19. Cai L, Johnstone BH, Cook TG, Tan J, Fishbein MC, Chen PS, March KL. IFATS collection: Human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells. 2009;27:230-237.
20. Amos PJ, Shang H, Bailey AM, Taylor A, Katz AJ, Peirce SM. IFATS collection: The role of human adipose-derived stromal cells in inflammatory microvascular remodeling and evidence of a perivascular phenotype. Stem Cells. 2008;26:2682-2690.
21. Traktuev DO, Merfeld-Clauss S, Li J, Kolonin M, Arap W, Pasqualini R, Johnstone BH, March KL. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res. 2008;102:77-85.
22. Rubina K, Kalinina N, Efimenko A, Lopatina T, Melikhova V, Tsokolaeva Z, Sysoeva V, Tkachuk V, Parfyonova Y. Adipose stromal cells stimulate angiogenesis via promoting progenitor cell differentiation, secretion of angiogenic factors, and enhancing vessel maturation. Tissue Eng Part A. 2009;15:2039-2050.
23. Butler MJ, Sefton MV. Cotransplantation of adipose-derived mesenchymal stromal cells and endothelial cells in a modular construct drives vascularization in SCID/bg mice. Tissue Eng Part A. 2012;18:1628-1641.
24. Szöke K, Beckstrøm KJ, Brinchmann JE. Human adipose tissue as a source of cells with angiogenic potential. Cell Transplant. 2012;21:235-250.
25. Merfeld-Clauss S, Gollahalli N, March KL, Traktuev DO. Adipose tissue progenitor cells directly interact with endothelial cells to induce vascular network formation. Tissue Eng Part A. 2010;16:2953-2966.
26. Hutton DL, Logsdon EA, Moore EM, Mac Gabhann F, Gimble JM, Grayson WL. Vascular morphogenesis of adipose-derived stem cells is mediated by heterotypic cell-cell interactions. Tissue Eng Part A. 2012;18:1729-1740.
27. Sarkanen JR, Vuorenpää H, Huttala O, Mannerström B, Kuokkanen H, Miettinen S, Heinonen T, Ylikomi T. Adipose stromal cell tubule network model provides a versatile tool for vascular research and tissue engineering. Cells Tissues Organs. 2012;196:385-397.
28. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, Pollok K, Ferkowicz MJ, Gilley D, Yoder MC. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104:2752-2760.
29. Riha GM, Wang X, Wang H, Chai H, Mu H, Lin PH, Lumsden AB, Yao Q, Chen C. Cyclic strain induces vascular smooth muscle cell differentiation from murine embryonic mesenchymal progenitor cells. Surgery. 2007;141:394-402.
30. Kobayashi N, Yasu T, Ueba H, Sata M, Hashimoto S, Kuroki M, Saito M, Kawakami M. Mechanical stress promotes the expression of smooth musclelike properties in marrow stromal cells. Exp Hematol. 2004;32:1238-1245.
31. Yamashita S, Maeshima A, Kojima I, Nojima Y. Activin A is a potent activator of renal interstitial fibroblasts. J Am Soc Nephrol. 2004;15:91-101.
32. Hirschi KK, Rohovsky SA, D'Amore PA. PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol. 1998;141:805-814.
33. McCarthy SA, Bicknell R. Inhibition of vascular endothelial cell growth by activin-A. J Biol Chem. 1993;268:23066-23071.
34. Merrilees MJ, Sodek J. Synthesis of TGF-beta 1 by vascular endothelial cells is correlated with cell spreading. J Vasc Res. 1992;29:376-384.
35. Song HY, Kim MY, Kim KH, Lee IH, Shin SH, Lee JS, Kim JH. Synovial fluid of patients with rheumatoid arthritis induces alpha-smooth muscle actin in human adipose tissue-derived mesenchymal stem cells through a TGF-beta1-dependent mechanism. Exp Mol Med. 2010;42:565-573.
36. Antonelli-Orlidge A, Saunders KB, Smith SR, D'Amore PA. An activated form of transforming growth factor beta is produced by cocultures of endothelial cells and pericytes. Proc Natl Acad Sci U S A. 1989;86:4544-4548.
37. Maeshima K, Maeshima A, Hayashi Y, Kishi S, Kojima I. Crucial role of activin a in tubulogenesis of endothelial cells induced by vascular endothelial growth factor. Endocrinology. 2004;145:3739-3745.
38. Zaragosi LE, Wdziekonski B, Villageois P, et al. Activin a plays a critical role in proliferation and differentiation of human adipose progenitors. Diabetes. 2010;59:2513-2521.
39. Gimble JM, Guilak F, Bunnell BA. Clinical and preclinical translation of cell-based therapies using adipose tissue-derived cells. Stem Cell Res Ther. 2010;1:19.