Bariatric surgery and diet-induced long-term caloric restriction protect subcutaneous adipose-derived stromal/progenitor cells and prolong their life span in formerly obese humans

Experimental Gerontology

Volumn 56, Issue , 2014, Pages 106-113

  Mitterberger, Maria C ^a   Mattesich, Monika ^b   Zwerschke, Werner ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Adipose derived stem cells; Caloric restriction; DNA damage; Humans; Senescence; Survival

Indexed keywords

DNA; FATTY ACID BINDING PROTEIN 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; FABP4 PROTEIN, HUMAN; FATTY ACID BINDING PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ADIPOGENESIS; ADIPOSE DERIVED STEM CELL; ADULT; ARTICLE; BARIATRIC SURGERY; CALORIC RESTRICTION; CELL DIFFERENTIATION; CELL DIVISION; CELL ISOLATION; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DNA DAMAGE; FEMALE; GASTRIC BANDING; HOMEOSTASIS; HUMAN; HUMAN CELL; NUCLEAR REPROGRAMMING; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH BYPASS; SUBCUTANEOUS FAT; WHITE ADIPOSE TISSUE; CASE CONTROL STUDY; CELL AGING; CELL CULTURE; CELL PROLIFERATION; LOW CALORY DIET; METABOLISM; MIDDLE AGED; NUTRITIONAL STATUS; PATHOLOGY; STEM CELL; STROMA CELL; TIME;

ADIPOGENESIS; ADULT; BARIATRIC SURGERY; CALORIC RESTRICTION; CASE-CONTROL STUDIES; CELL AGING; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DIET, REDUCING; DNA DAMAGE; FATTY ACID-BINDING PROTEINS; FEMALE; HUMANS; MIDDLE AGED; NUTRITIONAL STATUS; OBESITY; PPAR GAMMA; STEM CELLS; STROMAL CELLS; SUBCUTANEOUS FAT; TIME FACTORS;

EID: 84901834147     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.03.030     Document Type: Article

References (84)

1. Adams T.D., Gress R.E., Smith S.C., Halverson R.C., Simper S.C., Rosamond W.D., Lamonte M.J., Stroup A.M., Hunt S.C. Long-term mortality after gastric bypass surgery. N. Engl. J. Med. 2007, 357:753-761.
2. Alves H., Munoz-Najar U., De Wit J., Renard A.J., Hoeijmakers J.H., Sedivy J.M., Van Blitterswijk C., De Boer J. A link between the accumulation of DNA damage and loss of multi-potency of human mesenchymal stromal cells. J. Cell. Mol. Med. 2010, 14:2729-2738.
3. Ando K., Higami Y., Tsuchiya T., Kanematsu T., Shimokawa I. Impact of aging and life-long calorie restriction on expression of apoptosis-related genes in male F344 rat liver. Microsc. Res. Tech. 2002, 59:293-300.
4. Baker D.J., Perez-Terzic C., Jin F., Pitel K.S., Niederlander N.J., Jeganathan K., Yamada S., Reyes S., Rowe L., Hiddinga H.J., Eberhardt N.L., Terzic A., van Deursen J.M. Opposing roles for p16Ink4a and p19Arf in senescence and ageing caused by BubR1 insufficiency. Nat. Cell Biol. 2008, 10:825-836.
5. Baker D.J., Wijshake T., Tchkonia T., LeBrasseur N.K., Childs B.G., van de Sluis B., Kirkland J.L., van Deursen J.M. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 2011, 479:232-236.
6. Bartke A., Masternak M.M., Al-Regaiey K.A., Bonkowski M.S. Effects of dietary restriction on the expression of insulin-signaling-related genes in long-lived mutant mice. Interdiscip. Top. Gerontol. 2007, 35:69-82.
7. Bondolfi L., Ermini F., Long J.M., Ingram D.K., Jucker M. Impact of age and caloric restriction on neurogenesis in the dentate gyrus of C57BL/6 mice. Neurobiol. Aging 2004, 25:333-340.
8. Borkan G.A., Hults D.E., Gerzof S.G., Robbins A.H., Silbert C.K. Age changes in body composition revealed by computed tomography. J. Gerontol. 1983, 38:673-677.
9. Cawthorn W.P., Scheller E.L., MacDougald O.A. Adipose tissue stem cells meet preadipocyte commitment: going back to the future. J. Lipid Res. 2012, 53:227-246.
10. Cerletti M., Jang Y.C., Finley L.W., Haigis M.C., Wagers A.J. Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell 2012, 10:515-519.
11. Chen J., Astle C.M., Harrison D.E. Hematopoietic senescence is postponed and hematopoietic stem cell function is enhanced by dietary restriction. Exp. Hematol. 2003, 31:1097-1103.
12. Cinti S., Mitchell G., Barbatelli G., Murano I., Ceresi E., Faloia E., Wang S., Fortier M., Greenberg A.S., Obin M.S. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 2005, 46:2347-2355.
13. Cleary M.P., Brasel J.A., Greenwood M.R. Developmental changes in thymidine kinase, DNA, and fat cellularity in Zucker rats. Am. J. Physiol. 1979, 236:E508-E513.
14. Cohen H.Y., Miller C., Bitterman K.J., Wall N.R., Hekking B., Kessler B., Howitz K.T., Gorospe M., de Cabo R., Sinclair D.A. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 2004, 305:390-392.
15. Colman R.J., Anderson R.M., Johnson S.C., Kastman E.K., Kosmatka K.J., Beasley T.M., Allison D.B., Cruzen C., Simmons H.A., Kemnitz J.W., Weindruch R. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 2009, 325:201-204.
16. Cristancho A.G., Lazar M.A. Forming functional fat: a growing understanding of adipocyte differentiation. Nat. Rev. Mol. Cell Biol. 2011, 12:722-734.
17. D'Adda di Fagagna F. Living on a break: cellular senescence as a DNA-damage response. Nat. Rev. Cancer 2008, 8:512-522.
18. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9363-9367.
19. Dixon J.B., le Roux C.W., Rubino F., Zimmet P. Bariatric surgery for type 2 diabetes. Lancet 2012, 379:2300-2311.
20. Drolet R., Richard C., Sniderman A.D., Mailloux J., Fortier M., Huot C., Rheaume C., Tchernof A. Hypertrophy and hyperplasia of abdominal adipose tissues in women. Int. J. Obes. (Lond.) 2008, 32:283-291.
21. Ertl R.P., Chen J., Astle C.M., Duffy T.M., Harrison D.E. Effects of dietary restriction on hematopoietic stem-cell aging are genetically regulated. Blood 2008, 111:1709-1716.
22. Everitt A.V., Le Couteur D.G. Life extension by calorie restriction in humans. Ann. N. Y. Acad. Sci. 2007, 1114:428-433.
23. Faust I.M., Johnson P.R., Stern J.S., Hirsch J. Diet-induced adipocyte number increase in adult rats: a new model of obesity. Am. J. Physiol. 1978, 235:E279-E286.
24. Fazeli P.K., Bredella M.A., Misra M., Meenaghan E., Rosen C.J., Clemmons D.R., Breggia A., Miller K.K., Klibanski A. Preadipocyte factor-1 is associated with marrow adiposity and bone mineral density in women with anorexia nervosa. J. Clin. Endocrinol. Metab. 2010, 95:407-413.
25. Gesta S., Tseng Y.H., Kahn C.R. Developmental origin of fat: tracking obesity to its source. Cell 2007, 131:242-256.
26. Grillari J., Katinger H., Voglauer R. Contributions of DNA interstrand cross-links to aging of cells and organisms. Nucleic Acids Res. 2007, 35:7566-7576.
27. Harrison D.E., Archer J.R., Astle C.M. Effects of food restriction on aging: separation of food intake and adiposity. Proc. Natl. Acad. Sci. U. S. A. 1984, 81:1835-1838.
28. Hayflick L., Moorhead P.S. The serial cultivation of human diploid cell strains. Exp. Cell Res. 1961, 25:585-621.
29. Heilbronn L.K., de Jonge L., Frisard M.I., DeLany J.P., Larson-Meyer D.E., Rood J., Nguyen T., Martin C.K., Volaufova J., Most M.M., Greenway F.L., Smith S.R., Deutsch W.A., Williamson D.A., Ravussin E. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial. JAMA 2006, 295:1539-1548.
30. Hofer T., Fontana L., Anton S.D., Weiss E.P., Villareal D., Malayappan B., Leeuwenburgh C. Long-term effects of caloric restriction or exercise on DNA and RNA oxidation levels in white blood cells and urine in humans. Rejuvenation Res. 2008, 11:793-799.
31. Holloszy J.O. Mortality rate and longevity of food-restricted exercising male rats: a reevaluation. J. Appl. Physiol. 1997, 82:399-403.
32. Hudak C.S., Sul H.S. Pref-1, a gatekeeper of adipogenesis. Front. Endocrinol. 2013, 4:79.
33. Johnson J.E. Methods for studying cell death and viability in primary neuronal cultures. Methods Cell Biol. 1995, 46:243-276.
34. Johnson P.R., Hirsch J. Cellularity of adipose depots in six strains of genetically obese mice. J. Lipid Res. 1972, 13:2-11.
35. Kourtis N., Tavernarakis N. Cellular stress response pathways and ageing: intricate molecular relationships. EMBO J. 2011, 30:2520-2531.
36. Lee C.K., Klopp R.G., Weindruch R., Prolla T.A. Gene expression profile of aging and its retardation by caloric restriction. Science 1999, 285:1390-1393.
37. Lee J., Duan W., Long J.M., Ingram D.K., Mattson M.P. Dietary restriction increases the number of newly generated neural cells, and induces BDNF expression, in the dentate gyrus of rats. J. Mol. Neurosci. 2000, 15:99-108.
38. Lee J., Seroogy K.B., Mattson M.P. Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. J. Neurochem. 2002, 80:539-547.
39. Li Y., Yan Q., Pendergrass W.R., Wolf N.S. Response of lens epithelial cells to hydrogen peroxide stress and the protective effect of caloric restriction. Exp. Cell Res. 1998, 239:254-263.
40. Liao C.Y., Rikke B.A., Johnson T.E., Gelfond J.A., Diaz V., Nelson J.F. Fat maintenance is a predictor of the murine lifespan response to dietary restriction. Aging Cell 2011, 10:629-639.
41. Liao C.Y., Johnson T.E., Nelson J.F. Genetic variation in responses to dietary restriction - an unbiased tool for hypothesis testing. Exp. Gerontol. 2013, 48:1025-1029.
42. Lionaki E., Markaki M., Tavernarakis N. Autophagy and ageing: insights from invertebrate model organisms. Ageing Res. Rev. 2013, 12:413-428.
43. Liu L., Rando T.A. Aging of stem cells: intrinsic changes and environmental influences. Handbook of the Biology of Aging 2011, 141-161. Elsevier, The Netherlands, Amsterdam. Rando, E.J. Masoro, S.N. Austad (Eds.).
44. Lofgren P., Andersson I., Adolfsson B., Leijonhufvud B.M., Hertel K., Hoffstedt J., Arner P. Long-term prospective and controlled studies demonstrate adipose tissue hypercellularity and relative leptin deficiency in the postobese state. J. Clin. Endocrinol. Metab. 2005, 90:6207-6213.
45. López-Lluch G., Irusta P.M., Navas P., de Cabo R. Mitochondrial biogenesis and healthy aging. Exp. Gerontol. 2008, 43. (813-819).
46. Marchal J., Dal-Pan A., Epelbaum J., Blanc S., Mueller S., Wittig Kieffer M., Metzger F., Aujard F. Calorie restriction and resveratrol supplementation prevent age-related DNA and RNA oxidative damage in a non-human primate. Exp. Gerontol. 2013, 48:992-1000.
47. Masoro E.J. Overview of caloric restriction and ageing. Mech. Ageing Dev. 2005, 126:913-922.
48. Mattison J.A., Roth G.S., Beasley T.M., Tilmont E.M., Handy A.M., Herbert R.L., Longo D.L., Allison D.B., Young J.E., Bryant M., Barnard D., Ward W.F., Qi W., Ingram D.K., de Cabo R. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 2012, 489:318-321.
49. Migliaccio E., Giorgio M., Mele S., Pelicci G., Reboldi P., Pandolfi P.P., Lanfrancone L., Pelicci P.G. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 1999, 402:309-313.
50. Minamino T., Orimo M., Shimizu I., Kunieda T., Yokoyama M., Ito T., Nojima A., Nabetani A., Oike Y., Matsubara H., Ishikawa F., Komuro I. A crucial role for adipose tissue p53 in the regulation of insulin resistance. Nat. Med. 2009, 15:1082-1087.
51. Miranville A., Heeschen C., Sengenes C., Curat C.A., Busse R., Bouloumie A. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 2004, 110:349-355.
52. Mitterberger M.C., Zwerschke W. Mechanisms of resveratrol-induced inhibition of clonal expansion and terminal adipogenic differentiation in 3T3-L1 preadipocytes. J. Gerontol. A Biol. Sci. Med. Sci. 2013, 68:1356-1376.
53. Mitterberger M.C., Mattesich M., Klaver E., Lechner S., Engelhardt T., Larcher L., Pierer G., Piza-Katzer H., Zwerschke W. Adipokine profile and insulin sensitivity in formerly obese women subjected to bariatric surgery or diet-induced long-term caloric restriction. J. Gerontol. A Biol. Sci. Med. Sci. 2010, 65:915-923.
54. Mitterberger M.C., Lechner S., Mattesich M., Kaiser A., Probst D., Wenger N., Pierer G., Zwerschke W. DLK1(PREF1) is a negative regulator of adipogenesis in CD105(+)/CD90(+)/CD34(+)/CD31(-)/FABP4(-) adipose-derived stromal cells from subcutaneous abdominal fat pats of adult women. Stem Cell Res. 2012, 9:35-48.
55. Mitterberger M.C., Lechner S., Mattesich M., Zwerschke W. Adipogenic differentiation is impaired in replicative senescent human subcutaneous adipose-derived stromal/progenitor cells. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69:13-24.
56. O'Brien P.E., Dixon J.B., Laurie C., Skinner S., Proietto J., McNeil J., Strauss B., Marks S., Schachter L., Chapman L., Anderson M. Treatment of mild to moderate obesity with laparoscopic adjustable gastric banding or an intensive medical program: a randomized trial. Ann. Intern. Med. 2006, 144:625-633.
57. Park J.H., Glass Z., Sayed K., Michurina T.V., Lazutkin A., Mineyeva O., Velmeshev D., Ward W.F., Richardson A., Enikolopov G. Calorie restriction alleviates the age-related decrease in neural progenitor cell division in the aging brain. Eur. J. Neurosci. 2013, 37:1987-1993.
58. Rattan S.I. Hormesis in aging. Ageing Res. Rev. 2008, 7:63-78.
59. Redman L.M., Ravussin E. Caloric restriction in humans: impact on physiological, psychological, and behavioral outcomes. Antioxid. Redox Signal. 2011, 14:275-287.
60. Rodier F., Campisi J. Four faces of cellular senescence. J. Cell Biol. 2011, 192:547-556.
61. Rossi D.J., Bryder D., Seita J., Nussenzweig A., Hoeijmakers J., Weissman I.L. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 2007, 447:725-729.
62. Rubino F., Schauer P.R., Kaplan L.M., Cummings D.E. Metabolic surgery to treat type 2 diabetes: clinical outcomes and mechanisms of action. Annu. Rev. Med. 2010, 61:393-411.
63. Sedivy J.M., Munoz-Najar U.M., Jeyapalan J.C., Campisi J. Cellular senescence: a link between tumor suppression and organismal aging?. Molecular Biology of Aging 2008, 185-214. Cold Spring Harbor Laboratory Press, New York. L.P. Guarente, L. Partridge, D.C. Wallace (Eds.).
64. Sengenes C., Lolmede K., Zakaroff-Girard A., Busse R., Bouloumie A. Preadipocytes in the human subcutaneous adipose tissue display distinct features from the adult mesenchymal and hematopoietic stem cells. J. Cell. Physiol. 2005, 205:114-122.
65. Simons M.J., Koch W., Verhulst S. Dietary restriction of rodents decreases aging rate without affecting initial mortality rate - a meta-analysis. Aging Cell 2013, 12:410-414.
66. Sjostrom L., Narbro K., Sjostrom C.D., Karason K., Larsson B., Wedel H., Lystig T., Sullivan M., Bouchard C., Carlsson B., Bengtsson C., Dahlgren S., Gummesson A., Jacobson P., Karlsson J., Lindroos A.K., Lonroth H., Naslund I., Olbers T., Stenlof K., Torgerson J., Agren G., Carlsson L.M. Effects of bariatric surgery on mortality in Swedish obese subjects. N. Engl. J. Med. 2007, 357:741-752.
67. Sohal R.S., Agarwal S., Candas M., Forster M.J., Lal H. Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice. Mech. Ageing Dev. 1994, 76:215-224.
68. Spalding K.L., Arner E., Westermark P.O., Bernard S., Buchholz B.A., Bergmann O., Blomqvist L., Hoffstedt J., Naslund E., Britton T., Concha H., Hassan M., Ryden M., Frisen J., Arner P. Dynamics of fat cell turnover in humans. Nature 2008, 453:783-787.
69. Strissel K.J., Stancheva Z., Miyoshi H., Perfield J.W., DeFuria J., Jick Z., Greenberg A.S., Obin M.S. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 2007, 56:2910-2918.
70. Tchkonia T., Lenburg M., Thomou T., Giorgadze N., Frampton G., Pirtskhalava T., Cartwright A., Cartwright M., Flanagan J., Karagiannides I., Gerry N., Forse R.A., Tchoukalova Y., Jensen M.D., Pothoulakis C., Kirkland J.L. Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. Am. J. Physiol. Endocrinol. Metab. 2007, 292:E298-E307.
71. Tchkonia T., Morbeck D.E., Von Zglinicki T., Van Deursen J., Lustgarten J., Scrable H., Khosla S., Jensen M.D., Kirkland J.L. Fat tissue, aging, and cellular senescence. Aging Cell 2010, 9:667-684.
72. Tchoukalova Y.D., Koutsari C., Votruba S.B., Tchkonia T., Giorgadze N., Thomou T., Kirkland J.L., Jensen M.D. Sex- and depot-dependent differences in adipogenesis in normal-weight humans. Obesity (Silver Spring) 2010, 18:1875-1880.
73. Tchoukalova Y.D., Votruba S.B., Tchkonia T., Giorgadze N., Kirkland J.L., Jensen M.D. Regional differences in cellular mechanisms of adipose tissue gain with overfeeding. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18226-18231.
74. Turturro A., Witt W.W., Lewis S., Hass B.S., Lipman R.D., Hart R.W. Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program. J. Gerontol. A Biol. Sci. Med. Sci. 1999, 54:B492-B501.
75. van Harmelen V., Skurk T., Rohrig K., Lee Y.M., Halbleib M., Aprath-Husmann I., Hauner H. Effect of BMI and age on adipose tissue cellularity and differentiation capacity in women. Int. J. Obes. Relat. Metab. Disord. 2003, 27:889-895.
76. Vaquero A., Reinberg D. Calorie restriction and the exercise of chromatin. Genes Dev. 2009, 23:1849-1869.
77. Wang C., Maddick M., Miwa S., Jurk D., Czapiewski R., Saretzki G., Langie S.A., Godschalk R.W., Cameron K., von Zglinicki T. Adult-onset, short-term dietary restriction reduces cell senescence in mice. Aging (Albany NY) 2010, 2:555-566.
78. Weindruch R., Walford R.L. The Retardation of Aging and Disease by Dietary Restriction 1988, C.C. Thomas, Springfield, Ill., U.S.A.
79. Weindruch R., Walford R.L., Fligiel S., Guthrie D. The retardation of aging in mice by dietary restriction: longevity, cancer, immunity and lifetime energy intake. J. Nutr. 1986, 116:641-654.
80. Weindruch R., Colman R.J., Perez V., Richardson A.G. How does caloric restriction increase the longevity of mammals?. Molecular Biology of Aging 2008, 409-425. Cold Spring Harbor Laboratory Press, New York. L.P. Guarente, L. Partridge, D.C. Wallace (Eds.).
81. Wolf N.S., Pendergrass W.R. The relationships of animal age and caloric intake to cellular replication in vivo and in vitro: a review. J. Gerontol. A Biol. Sci. Med. Sci. 1999, 54:B502-B517.
82. Yilmaz O.H., Katajisto P., Lamming D.W., Gultekin Y., Bauer-Rowe K.E., Sengupta S., Birsoy K., Dursun A., Yilmaz V.O., Selig M., Nielsen G.P., Mino-Kenudson M., Zukerberg L.R., Bhan A.K., Deshpande V., Sabatini D.M. mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 2012, 486:490-495.
83. Yu B.P. Antioxidant action of dietary restriction in the aging process. J. Nutr. Sci. Vitaminol. (Tokyo) 1993, 39(Suppl.):S75-S83.
84. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372:425-432.