Multipotent stromal cells are activated to reduce apoptosis in part by upregulation and secretion of stanniocalcin-1

Stem Cells

Volumn 27, Issue 3, 2009, Pages 670-681

  Block, Gregory J ^a   Ohkouchi, Shinya ^a   Fung, France ^a   Frenkel, Joshua ^a   Gregory, Carl ^a   Pochampally, Radhika ^a   Dimattia, Gabriel ^b   Sullivan, Deborah E ^c   Prockop, Darwin J ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis, ischemia; Microarray; Multipotent stromal cells; Stanniocalcin 1; UV irradiation

Indexed keywords

HYPOCALCIN; STANNIOCALCIN 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL CULTURE; CONTROLLED STUDY; EPITHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; MULTIPOTENT STEM CELL; NUCLEOTIDE SEQUENCE; PROTEIN SECRETION; PROTEIN SYNTHESIS; STROMA CELL; ULTRAVIOLET IRRADIATION; UPREGULATION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; FIBROBLASTS; GLYCOPROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; MICE; MICROSCOPY, FLUORESCENCE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STROMAL CELLS; TRANSFECTION; ULTRAVIOLET RAYS; UP-REGULATION;

EID: 65249161144     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2008-0742     Document Type: Article

References (45)

1. Owen M, Friedenstein AJ. Stromal stem cells: Marrow-derived osteogenic precursors. Ciba Found Symp 1988;136:42-60.
2. Owen M. Marrow stromal stem cells. J Cell Sci 1988;10:63-76.
3. Spees JL, Olson SD, Ylostalo J et al. Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epithelium by human adult stem cells from bone marrow stroma. Proc Natl Acad Sci USA 2003;100:2397-2402.
4. Chopp M, Zhang XH, Li Y et al. Spinal cord injury in rat: Treatment with bone marrow stromal cell transplantation. Neuroreport 2000;11: 3001-3005.
5. Horwitz EM, Gordon PL, Koo WK et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci U S A 2002;99:8932-8937.
6. Iso Y, Spees JL, Serrano C et al. Multipotent human stromal cells improve cardiac function after myocardial infarction in mice without long-term engraftment. Biochem Biophys Res Commun 2007;354:700-706.
7. Munoz JR, Stoutenger BR, Robinson AP et al. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci USA 2005;102:18171-18176.
8. Lee RH, Hsu SC, Munoz J et al. A subset of human rapidly self- renewing marrow stromal cells preferentially engraft in mice. Blood 2006;107:2153-2161.
9. Le Blanc K. Mesenchymal stromal cells: Tissue repair and immune modulation. Cytotherapy 2006;8:559-561.
10. Ortiz LA, Dutreil M, Fattman C et al. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchy- mal stem cells during lung injury. Proc Natl Acad Sci U S A 2007; 104:11002-11007.
11. Gupta N, Su X, Popov B et al. Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endo- toxin-induced acute lung injury in mice. J Immunol 2007;179:1855-1863.
12. Xu G, Zhang L, Ren G et al. Immunosuppressive properties of cloned bone marrow mesenchymal stem cells. Cell Res 2007;17:240-248.
13. Noiseux N, Gnecchi M, Lopez-Ilasaca M et al. Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation. Mol Ther 2006;14:840-850.
14. Mirotsou M, Zhang Z, Deb A et al. Secreted frizzled related protein 2 (Sfrp2) is the key Akt-mesenchymal stem cell-released paracrine factor mediating myocardial survival and repair. Proc Natl Acad Sci U S A 2007;104:1643-1648.
15. Hung SC, Pochampally RR, Chen SC et al. Angiogenic effects of human multipotent stromal cells (MSCs)-conditioned medium activates the PI3K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis, increase survival, and stimulate angiogenesis. Stem Cells 2007;25:2363-2370.
16. Westberg JA, Serlachius M, Lankila P et al. Hypoxic preconditioning induces neuroprotective stanniocalcin-1 in brain via IL-6 signaling. Stroke 2007;38:1025-1030.
17. Westberg JA, Serlachius M, Lankila P et al. Hypoxic preconditioning induces elevated expression of stanniocalcin-1 in the heart. Am J Physiol Heart Circ Physiol 2007;293:H1766-H1771.
18. Teplova V, Jaaskelainen E, Salkinoja-Salonen M et al. Differentiated Paju cells have increased resistance to toxic effects of potassium ionophores. Acta Bioch Pol 2004;51:539-544.
19. Koizumi K, Hoshiai M, Ishida H et al. Stanniocalcin 1 prevents cytosolic Ca2+ overload and cell hypercontracture in cardiomyocytes. Circ J 2007;71:796-801.
20. Ellard JP, McCudden CR, Tanega C et al. The respiratory effects of stanniocalcin-1 (STC-1) on intact mitochondria and cells: STC-1 uncouples oxidative phosphorylation and its actions are modulated by nucleotide triphosphates. Mol Cell Endocrinol 2007;264:90-101.
21. Chakraborty A, Brooks H, Zhang P et al. Stanniocalcin-1 regulates endothelial gene expression and modulates transendothelial migration of leukocytes. Am J Physiol 2007;292:F895-F904.
22. Sekiya I, Larson BL, Smith JR et al. Expansion of human adult stem cells from bone marrow stroma: Conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 2002;20:530-541.
23. Larson BL, Ylostalo J, Prockop DJ. Human multipotent stromal cells undergo sharp transition from division to development in culture. Stem Cells 2008;26:193-201.
24. Ylostalo J, Smith JR, Pochampally RR et al. Use of differentiating adult stem cells (marrow stromal cells) to identify new downstream target genes for transcription factors. Stem Cells 2006;24:642-652.
25. Li C, Wong WH. Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc Natl Acad Sci U S A 2001;98:31-36.
26. Schindl A, Klosner G, Honigsmann H et al. Flow cytometric quantification of UV-induced cell death in a human squamous cell carcinoma-derived cell line: Dose and kinetic studies. J Photochem Photobiol B 1998;44:97-106.
27. Wilkins RC, Kutzner BC, Truong M et al. Analysis of radiation- induced apoptosis in human lymphocytes: Flow cytometry using Annexin V and propidium iodide versus the neutral comet assay. Cytometry 2002;48:14-19.
28. Zhan Q, Jin S, Ng B et al. Caspase-3 mediated cleavage of BRCA1 during UV-induced apoptosis. Oncogene 2002;21:5335-5345.
29. Varghese R, Gagliardi AD, Bialek PE et al. Overexpression of human stanniocalcin affects growth and reproduction in transgenic mice. Endocrinology 2002;143:868-876.
30. Graham RM, Frazier DP, Thompson JW et al. A unique pathway of cardiac myocyte death caused by hypoxia-acidosis. J Exp Biol 2004; 207:3189-3200.
31. Kim JS, Jin Y, Lemasters JJ. Reactive oxygen species, but not Ca2+ overloading, trigger pH- and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion. Am J Physiol Heart Circ Physiol 2006;290:H2024-H2034.
32. Gladden LB. Lactic acid: New roles in a new millennium. Proc Natl Acad Sci U S A 2001;98:395-397.
33. Sazonova O, James KA, McCudden CR et al. Stanniocalcin-1 secretion and receptor regulation in kidney cells. Am J Physiol 2008;294:F788-F794.
34. Block GJ, Eskiw CH, Dellaire G et al. Transcriptional regulation is affected by subnuclear targeting of reporter plasmids to PML nuclear bodies. Mol Cell Biol 2006;26:8814-8825.
35. Mouiseddine M, Francois S, Semont A et al. Human mesenchymal stem cells home specifically to radiation-injured tissues in a non-obese diabetes/severe combined immunodeficiency mouse model. Br J Radiol 2007;80(spec. no. 1):S49-S55.
36. Zlot C, Ingle G, Hongo J et al. Stanniocalcin 1 is an autocrine modulator of endothelial angiogenic responses to hepatocyte growth factor. J Biol Chem 2003;278:47654-47659.
37. Kanellis J, Bick R, Garcia G et al. Stanniocalcin-1, an inhibitor of macrophage chemotaxis and chemokinesis. Am J Physiol 2004;286: F356-F362.
38. Yeung HY, Lai KP, Chan HY et al. Hypoxia-inducible factor-1-mediated activation of stanniocalcin-1 in human cancer cells. Endocrinology 2005;146:4951-4960.
39. McCudden CR, James KA, Hasilo C et al. Characterization of mammalian stanniocalcin receptors. Mitochondrial targeting of ligand and receptor for regulation of cellular metabolism. J Biol Chem 2002;277: 45249-45258.
40. Sheikh-Hamad D, Bick R, Wu GY et al. Stanniocalcin-1 is a naturally occurring L-channel inhibitor in cardiomyocytes: Relevance to human heart failure. Am J Physiol Heart Circ Physiol 2003;285: H442-H448.
41. Hasilo CP, McCudden CR, Gillespie JR et al. Nuclear targeting of stanniocalcin to mammary gland alveolar cells during pregnancy and lactation. Am J Physiol 2005;289:E634-E642.
42. Zhang K, Lindsberg PJ, Tatlisumak T et al. Stanniocalcin: A molecular guard of neurons during cerebral ischemia. Proc Natl Acad Sci U S A 2000;97:3637-3642.
43. Holmes DI, Zachary IC. Vascular endothelial growth factor regulates Stanniocalcin-1 expression via Neuropilin-1-dependent regulation of KDR and synergism with fibroblast growth Factor-2. Cell Signal 2008;20:569-579.
44. Wu S, Yoshiko Y, De Luca F. Stanniocalcin 1 acts as a paracrine regulator of growth plate chondrogenesis. J Biol Chem 2006;281:5120-5127.
45. Filvaroff EH, Guillet S, Zlot C et al. Stanniocalcin 1 alters muscle and bone structure and function in transgenic mice. Endocrinology 2002;143:3681-3690.