Human mesenchymal stem cells/multipotent stromal cells consume accumulated autophagosomes early in differentiation

Stem Cell Research and Therapy

Volumn 5, Issue 6, 2014, Pages

  Nuschke, Austin ^a,b   Rodrigues, Melanie ^a   Stolz, Donna B ^a,b   Chu, Charleen T ^a   Griffith, Linda ^c   Wells, Alan ^a,b,d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b MCGOWAN INSTITUTE FOR REGENERATIVE MEDICINE   (United States)

^c Massachusetts Institute of Technology   (United States)

^d Department of Biological Engineering Massachusetts Institute of Technology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAFILOMYCIN; GREEN FLUORESCENT PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1; RAPAMYCIN; RED FLUORESCENT PROTEIN;

ADIPOGENESIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BIOACCUMULATION; BIODEGRADATION; BIOLOGICAL MONITORING; BONE DEVELOPMENT; CELL CYCLE ARREST; CELL DIFFERENTIATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LIGHT CHAIN; LIPID STORAGE; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; MULTIPOTENT STROMA CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN METABOLISM; QUANTITATIVE ANALYSIS; ROUGH ENDOPLASMIC RETICULUM; STAINING; STROMA CELL; TRANSMISSION ELECTRON MICROSCOPY; CELL CULTURE; CYTOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; PHAGOSOME; ULTRASTRUCTURE;

MAMMALIA;

AUTOPHAGY; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MESENCHYMAL STROMAL CELLS; PHAGOSOMES;

EID: 84927778158     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt530     Document Type: Article

References (33)

1. Pittenger M, Mackay A, Beck S, Jaiswal R, Douglas R, Mosca J, Moorman M, Simonetti D, Craig S, Marshak D: Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
2. Bianco P, Riminucci M, Gronthos S, Robey P: Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 2001, 19:180-192.
3. Pereira R, Halford K, O'Hara M, Leeper D, Sokolov B, Pollard M, Bagasra O, Prockop D: 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, 92:4857-4861.
4. Kim DH, Yoo KH, Choi KS, Choi J, Choi SY, Yang SE, Yang YS, Im HJ, Kim KH, Jung HL, Sung KW, Koo HH: Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine 2005, 31:119-126.
5. Rodrigues M, Turner O, Stolz D, Griffith L, Wells A: Production of reactive oxygen species by multipotent stromal cells/mesenchymal stem cells upon exposure to Fas Ligand. Cell Transplant 2012, 21:16.
6. Zhu W, Chen J, Cong X, Hu S, Chen X: Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells. Stem Cells 2006, 24:416-425.
7. Kim W-K, Meliton V, Bourquard N, Hahn T, Parhami F: Hedgehog signaling and osteogenic differentiation in multipotent bone marrow stromal cells are inhibited by oxidative stress. J Cell Biochem 2010, 111:1199-1209.
8. Rodrigues M, Griffith L, Wells A: Growth factor regulation of proliferation and survival of multipotential stromal cells. Stem Cell Res Ther 2010, 1:32.
9. Falanga V, Iwamoto S, Chartier M, Yufit T, Butmarc J, Kouttab N, Shrayer D, Carson P: Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng 2007, 13:1299-1312.
10. Lu D, Chen B, Liang Z, Deng W, Jiang Y, Li S, Xu J, Wu Q, Zhang Z, Xie B, Chen S: 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.
11. Wang L, Pasha Z, Wang S, Li N, Feng Y, Lu G, Millard R, Ashraf M: Protein kinase G1 α overexpression increases stem cell survival and cardiac function after myocardial infarction. PLoS One 2013, 8:e60087.
12. Williams AR, Suncion VY, McCall F, Guerra D, Mather J, Zambrano JP, Heldman AW, Hare JM: Durable scar size reduction due to allogeneic mesenchymal stem cell therapy regulates whole-chamber remodeling. J Am Heart Assoc 2013, 2:e000140.
13. Papandreou I, Lim A, Laderoute K, Denko N: Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L. Cell Death Differ 2008, 15:1572-1581.
14. Rabinowitz J, White E: Autophagy and metabolism. Science 2010, 330:1344-1348.
15. Mizushima N, Levine B: Autophagy in mammalian development and differentiation. Nat Cell Biol 2010, 12:823-830.
16. Zhang Q, Yang Y-J, Wang H, Dong Q-T, Wang T-J, Qian H-Y, Xu H: Autophagy activation: a novel mechanism of atorvastatin to protect mesenchymal stem cells from hypoxia and serum deprivation via AMP-activated protein kinase/mammalian target of rapamycin pathway. Stem Cells Dev 2012, 21:1321-1332.
17. Oliver L, Hue E, Priault M, Vallette F: Basal autophagy decreased during the differentiation of human adult mesenchymal stem cells. Stem Cells Dev 2012, 21:2779-2788.
18. Pantovic A, Krstic A, Janjetovic K, Kocic J, Harhaji-Trajkovic L, Bugarski D, Trajkovic V: Coordinated time-dependent modulation of AMPK/Akt/mTOR signaling and autophagy controls osteogenic differentiation of human mesenchymal stem cells. Bone 2013, 52:7.
19. Stolz D, Ross M, Salem H, Mars W, Michalopoulos G, Enomoto K: Cationic colloidal silica membrane perturbation as a means of examining changes at the sinusoidal surface during liver regeneration. Am J Pathol 1999, 155:1487-1498.
20. Degasperi A, Birtwistle MR, Volinsky N, Rauch J, Kolch W, Kholodenko BN: Evaluating strategies to normalise biological replicates of western blot data. PLoS One 2014, 9:e87293.
21. Kimura S, Noda T, Yoshimori T: Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007, 3:452-460.
22. Funes J, Quintero M, Henderson S, Martinez D, Qureshi U, Westwood C, Clements M, Bourboulia D, Pedley R, Moncada S, Boshoff C: Transformation of human mesenchymal stem cells increases their dependency on oxidative phosphorylation for energy production. Proc Natl Acad Sci U S A 2007, 104:6223-6228.
23. Pattappa G, Heywood HK, de Bruijn JD, Lee DA: The metabolism of human mesenchymal stem cells during proliferation and differentiation. J Cell Physiol 2011, 226:2562-2570.
24. Shigemitsu K, Tsujishita Y, Hara K, Nanahoshi M, Avruch J, Yonezawa K: Regulation of translational effectors by amino acid and mammalian target of rapamycin signaling pathways. Possible involvement of autophagy in cultured hepatoma cells. J Biol Chem 1999, 274:1058-1065.
25. Codogno P, Mehrpour M, Proikas-Cezanne T: Canonical and non-canonical autophagy: variations on a common theme of self-eating? Nat Rev Mol Cell Biol 2012, 13:7-12.
26. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T: LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000, 19:5720-5728.
27. Klionsky D, Abeliovich H, Agostinis P, Agrawal D, Aliev G, Askew D, Baba M, Baehrecke E, Bahr B, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, Biard-Piechaczyk M, Blum JS, Bredesen DE, Brodsky JL, Brumell JH, Brunk UT, Bursch W, Camougrand N, Cebollero E, Cecconi F, Chen Y, Chin LS, Choi A, Chu CT, Chung J, Clarke PG, et al: Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4:151-175.
28. Singh R, Xiang Y, Wang Y, Baikati K, Cuervo AM, Luu YK, Tang Y, Pessin JE, Schwartz GJ, Czaja MJ: Autophagy regulates adipose mass and differentiation in mice. J Clin Invest 2009, 119:3329-3339.
29. Zhang Y, Goldman S, Baerga R, Zhao Y, Komatsu M, Jin S: Adipose-specific deletion of autophagy-related gene 7 (atg7) in mice reveals a role in adipogenesis. Proc Natl Acad Sci U S A 2009, 106:19860-19865.
30. Tra T, Gong L, Kao L-P, Li X-L, Grandela C, Devenish R, Wolvetang E, Prescott M: Autophagy in human embryonic stem cells. PLoS One 2011, 6:e27485.
31. Chen T, Shen L, Yu J, Wan H, Guo A, Chen J, Long Y, Zhao J, Pei G: Rapamycin and other longevity-promoting compounds enhance the generation of mouse induced pluripotent stem cells. Aging Cell 2011, 10:908-911.
32. Menendez J, Vellon L, Oliveras-Ferraros C, Cufí S, Vazquez-Martin A: mTOR-regulated senescence and autophagy during reprogramming of somatic cells to pluripotency: a roadmap from energy metabolism to stem cell renewal and aging. Cell Cycle 2011, 10:3658-3677.
33. Mylotte L, Duffy A, Murphy M, O'Brien T, Samali A, Barry F, Szegezdi E: Metabolic flexibility permits mesenchymal stem cell survival in an ischemic environment. Stem Cells 2008, 26:1325-1336.