High Aldehyde Dehydrogenase Activity Identifies a Subset of Human Mesenchymal Stromal Cells with Vascular Regenerative Potential

Stem Cells

Volumn 35, Issue 6, 2017, Pages 1542-1553

  Sherman, Stephen E ^a,b   Kuljanin, Miljan ^b   Cooper, Tyler T ^a,b   Putman, David M ^a,b   Lajoie, Gilles A ^b   Hess, David A ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b WESTERN UNIVERSITY   (Canada)

Author keywords

Aldehyde dehydrogenase; Angiogenesis; Multipotent stromal cells; Peripheral artery disease; Proteomics; Transplantation

Indexed keywords

5' NUCLEOTIDASE; ALDEHYDE DEHYDROGENASE; ANGIOGENIN; CD14 ANTIGEN; CD146 ANTIGEN; CD45 ANTIGEN; ENDOGLIN; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; THY 1 ANTIGEN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; BIOLOGICAL MARKER; PROTEOME;

ANIMAL CELL; APOPTOSIS; ARTICLE; CAPILLARY ENDOTHELIAL CELL; CELL CONTACT; CELL DIFFERENTIATION; CELL EXPANSION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MASS SPECTROMETRY; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; PHENOTYPE; ANGIOGENESIS; BLOOD VESSEL; BLOOD VESSEL PROSTHESIS; CONDITIONED MEDIUM; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; ENZYMOLOGY; GENETICS; METABOLISM; MICROVASCULATURE; MULTIPOTENT STEM CELL; PERICYTE; PHARMACOLOGY; PHYSIOLOGY; REGENERATION; SECRETION (PROCESS); STROMA CELL;

ALDEHYDE DEHYDROGENASE; BIOMARKERS; BLOOD VESSEL PROSTHESIS; BLOOD VESSELS; CELL DIFFERENTIATION; CELL PROLIFERATION; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; ENDOTHELIAL CELLS; HUMANS; MESENCHYMAL STROMAL CELLS; MICROVESSELS; MULTIPOTENT STEM CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; PERICYTES; PROTEOME; REGENERATION; RNA, MESSENGER; STROMAL CELLS;

EID: 85017166914     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2612     Document Type: Article

References (44)

1. Fowkes FGR, Rudan D, Rudan I et al. Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: A systematic review and analysis. Lancet 2013;382:1329–1340.
2. Criqui MH, Aboyans V. Epidemiology of peripheral artery disease. Circ Res 2015;116:1509–1526.
3. Lawall H, Bramlage P, Amann B. Treatment of peripheral arterial disease using stem and progenitor cell therapy. J Vasc Surg 2011;53:445–453.
4. Makowsky M, McMurtry MS, Elton T et al. Prevalence and treatment patterns of lower extremity peripheral arterial disease among patients at risk in ambulatory health settings. Can J Cardiol 2011;27:389.e311–389.e388.
5. Davies JE. Criticial limb ischemia: Epidemiology. Methodist Debakey Cardiovasc J 2012;8:10–14.
6. Tateishi-Yuyama E, Matsubara H, Murohara T et al. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: A pilot study and a randomised controlled trial. Lancet 2002;360:427–435.
7. Matoba S, Tatsumi T, Murohara T et al. Long-term clinical outcome after intramuscular implantation of bone marrow mononuclear cells (Therapeutic Angiogenesis by Cell Transplantation [TACT] trial) in patients with chronic limb ischemia. Am Heart J 2008;156:1010–1018.
8. Fadini GP, Losordo D, Dimmeler S. Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 2012;110:624–637.
9. Storms RW, Trujillo AP, Springer JB et al. Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci USA 1999;96:9118–9123.
10. Capoccia BJ, Robson DL, Levac KD et al. Revascularization of ischemic limbs after transplantation of human bone marrow cells with high aldehyde dehydrogenase activity. Blood 2009;113:5340–5351.
11. Hess DA, Meyerrose TE, Wirthlin L et al. Functional characterization of highly purified human hematopoietic repopulating cells isolated according to aldehyde dehydrogenase activity. Blood 2004;104:1648–1655.
12. Hess DA, Craft TP, Wirthlin L et al. Widespread nonhematopoietic tissue distribution by transplanted human progenitor cells with high aldehyde dehydrogenase activity. Stem Cells 2008;26:611–620.
13. Bell GI, Broughton HC, Levac KD et al. Transplanted human bone marrow progenitor subtypes stimulate endogenous islet regeneration and revascularization. Stem Cells Dev 2012;21:97–109.
14. Bell GI, Putman DM, Hughes-Large JM et al. Intrapancreatic delivery of human umbilical cord blood aldehyde dehydrogenase-producing cells promotes islet regeneration. Diabetologia 2012;55:1755–1760.
15. Putman DM, Liu KY, Broughton HC et al. Umbilical cord blood-derived aldehyde dehydrogenase-expressing progenitor cells promote recovery from acute ischemic injury. Stem Cells 2012;30:2248–2260.
16. Perin EC, Murphy M, Cooke JP et al. Rationale and design for PACE: Patients with intermittent claudication injected with ALDH bright cells. Am Heart J 2014;168:667–673.
17. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315–317.
18. Maitra B, Szekely E, Gjini K et al. Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplantation 2004;33:597–604.
19. Salem HK, Thiemermann C. Mesenchymal stromal cells: Current understanding and clinical status. Stem Cells 2010;28:585–596.
20. Si Y, Zhao Y, Hao H et al. Infusion of mesenchymal stem cells ameliorates hyperglycemia in type 2 diabetic rats: Identification of a novel role in improving insulin sensitivity. Diabetes 2012;61:1616–1625.
21. Caplan AI, Correa D. The MSC: An injury drugstore. Cell Stem Cell 2011;9:11–15.
22. Hung SC, Pochampally RR, Chen SC et al. Angiogenic effects of human multipotent stromal cell conditioned medium activate the PI3K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis, increase survival, and stimulate angiogenesis. Stem Cells 2007;25:2363–2370.
23. Al-Khaldi A, Al-Sabti H, Galipeau J et al. Therapeutic angiogeneis using autologous bone marrow stromal cells: Improved blood flow in a Chronic Limb Ischemia model. Ann Thorac Surg 2003;75:6.
24. Melero-Martin JM, De Obaldia ME, Kang SY et al. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 2008;103:194–202.
25. Ball SG, Shuttleworth CA Kielty CM. Mesenchymal stem cells and neovascularization: Role of platelet-derived growth factor receptors. J Cell Mol Med 2007;11:1012–1030.
26. Au P, Tam J, Fukumura D et al. Bone marrow derived mesenchymal stem cells facilitate engineering of long lasting functional vasculature. Blood 2008;111:
27. Liew A O'brien T. Therapeutic potential for mesenchymal stem cell transplantation in critical limb ischemia. Stem Cell Res Ther 2012;3:28.
28. Gupta PK, Chullikana A, Parakh R et al. A double blind randomized placebo controlled phase I/II study assessing the safety and efficacy of allogeneic bone marrow derived mesenchymal stem cell in critical limb ischemia. J Transl Med 2013;11:143.
29. Dash NR, Dash SN, Routray P et al. Targeting nonhealing ulcers of lower extremity in human through autologous bone marrow-derived MSC. Rejuvenation Res 2009;12:8.
30. Lasala GP, Silva JA, Gardner PA et al. Combination stem cell therapy for the treatment of severe limb ischemia: Safety and efficacy analysis. Angiology 2010;61:551–556.
31. Lasala GP, Silva JA, Minguell JJ. Therapeutic angiogenesis in patients with severe limb ischemia by transplantation of a combination stem cell product. J Thorac Cardiovasc Surg 2012;144:377–382.
32. Lu D, Chen B, Liang Z et al. Comparison of bone marrow mesenchymal stem cells with bone marrow-derived mononuclear cells for treatment of diabetic critical limb ischemia and foot ulcer: A double-blind, randomized, controlled trial. Diabetes Res Clin Pract 2011;92:26–36.
33. Putman DM, Hess DA. Isolation of human umbilical cord blood aldehyde dehydrogenase-expressing progenitor cells that modulate vascular regenerative functions in vitro and in vivo. Curr Protoc Stem Cell Biol 2013;Chapter 2:Unit 2A 10.
34. Bendall SC, Booy AT, Lajoie G. Proteomic analysis of pluripotent stem cells. In: Current Protocols in Stem Cell Biology. Wiley, Hoboken, NJ, 2007.
35. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized ppb-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008;26:1367–1372.
36. Consortium U. UniProt: A hub for protein information. Nucleic Acids Res 2014;gku989.
37. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815–1822.
38. Bernardo ME, Fibbe WE. Mesenchymal stromal cells: Sensors and switchers of inflammation. Cell Stem Cell 2013;13:392–402.
39. Melief SM, Schrama E, Brugman MH et al. Multipotent stromal cells induce human regulatory T cells through a novel pathway involving skewing of monocytes toward anti-inflammatory macrophages. Stem Cells 2013;31:1980–1991.
40. Dhahri D, Sato-Kusubata K, Ohki-Koizumi M et al. Fibrinolytic factor-mediated crosstalk with endothelial cells expands murine bone marrow mesenchymal stromal cells. Blood 2016;blood-2015-2010-673103.
41. Wang Z, Huang H. Platelet factor-4 (CXCL4/PF-4): An angiostatic chemokine for cancer therapy. Cancer Lett 2013;331:147–153.
42. O'Reilly MS, Holmgren L, Shing Y et al. Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastases by a lewis lung carcinoma. Cell 1994;79:315–328.
43. Dudani AK, Ben-Tchavtchavadze M, Porter S et al. Angiostatin and plasminogen share binding to endothelial cell surface actin. Biochem Cell Biol 2005;83:28–35.
44. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996;86:353–364.