Systemic attenuation of the TGF-β pathway by a single drug simultaneously rejuvenates hippocampal neurogenesis and myogenesis in the same old mammal

Oncotarget

Volumn 6, Issue 14, 2015, Pages 11959-11978

  Yousef, Hanadie ^b,c   Conboy, Michael J ^a   Morgenthaler, Adam ^a   Schlesinger, Christina ^a   Bugaj, Lukasz ^a   Paliwal, Preeti ^a   Greer, Christopher ^a   Conboy, Irina M ^a   Schaffer, David ^a,b  

^a University of California   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Aging; Myogenesis; Neurogenesis; Stem cell microenvironment; TGF signaling

Indexed keywords

2 [3 (6 METHYLPYRIDIN 2 YL) 1H PYRAZOL 4 YL] 1,5 NAPHTHYRIDINE; BETA 2 MICROGLOBULIN; BROXURIDINE; EDOXUDINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN TYROSINE KINASE INHIBITOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; MICROGLIA; MOUSE; MUSCLE DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STEM CELL NICHE; TISSUE REGENERATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; FEMALE; FISCHER 344 RAT; IMMUNOHISTOCHEMISTRY; NEURAL STEM CELL; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RAT; WESTERN BLOTTING;

AGING; ANIMALS; BLOTTING, WESTERN; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MUSCLE DEVELOPMENT; NEURAL STEM CELLS; NEUROGENESIS; POLYMERASE CHAIN REACTION; RATS; RATS, INBRED F344; STEM CELL NICHE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84931477439     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3851     Document Type: Article

References (69)

1. Conboy IM, Rando TA. Heterochronic parabiosis for the study of the effects of aging on stem cells and their niches. Cell cycle (Georgetown, Tex). 2012; 11:2260-2267.
2. Silva HS, Conboy IM, Gilliland G. (2008). Aging and stem cell renewal. StemBook: The Stem Cell Research Community.
3. Loffredo FS, Steinhauser ML, Jay SM, Gannon J, Pancoast JR, Yalamanchi P, Sinha M, Dall'Osso C, Khong D, Shadrach JL, Miller CM, Singer BS, Stewart A, Psychogios N, Gerszten RE, Hartigan AJ, et al. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell. 2013; 153:828-839.
4. Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, Stan TM, Fainberg N, Ding Z, Eggel A, Lucin KM, Czirr E, Park JS, Couillard-Despres S, Aigner L, Li G, et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature. 2011; 477:90-94.
5. Vukovic J, Colditz MJ, Blackmore DG, Ruitenberg MJ, Bartlett PF. Microglia modulate hippocampal neural precursor activity in response to exercise and aging. J Neurosci. 2012; 32:6435-6443.
6. Carlson ME, Conboy MJ, Hsu M, Barchas L, Jeong J, Agrawal A, Mikels AJ, Agrawal S, Schaffer DV, Conboy IM. Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging cell. 2009; 8:676-689.
7. Paliwal P, Pishesha N, Wijaya D, Conboy IM. Age dependent increase in the levels of osteopontin inhibits skeletal muscle regeneration. Aging. 2012; 4:553-566.
8. Ruckh JM, Zhao JW, Shadrach JL, van Wijngaarden P, Rao TN, Wagers AJ, Franklin RJ. Rejuvenation of regeneration in the aging central nervous system. Cell stem cell. 2012; 10:96-103.
9. Katsimpardi L, Litterman NK, Schein PA, Miller CM, Loffredo FS, Wojtkiewicz GR, Chen JW, Lee RT, Wagers AJ, Rubin LL. Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science (New York, NY). 2014; 344:630-634.
10. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nature reviews Neuroscience. 2010; 11:339-350.
11. Deng W, Saxe MD, Gallina IS, Gage FH. Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci. 2009; 29:13532-13542.
12. Oboti L, Savalli G, Giachino C, De Marchis S, Panzica GC, Fasolo A, Peretto P. Integration and sensory experiencedependent survival of newly-generated neurons in the accessory olfactory bulb of female mice. The European journal of neuroscience. 2009; 29:679-692.
13. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC. Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci. 2004; 24:1726-1733.
14. Olariu A, Cleaver KM, Cameron HA. Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. The Journal of comparative neurology. 2007; 501:659-667.
15. Walter J, Keiner S, Witte OW, Redecker C. Age-related effects on hippocampal precursor cell subpopulations and neurogenesis. Neurobiology of aging. 2011; 32:1906-1914.
16. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. Neurogenesis in the adult human hippocampus. Nature medicine. 1998; 4:1313-1317.
17. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Bostrom E, Westerlund I, Vial C, Buchholz BA, Possnert G, Mash DC, Druid H, Frisen J. Dynamics of hippocampal neurogenesis in adult humans. Cell. 2013; 153:1219-1227.
18. Bergmann O, Liebl J, Bernard S, Alkass K, Yeung MS, Steier P, Kutschera W, Johnson L, Landen M, Druid H, Spalding KL, Frisen J. The age of olfactory bulb neurons in humans. Neuron. 2012; 74:634-639.
19. Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science (New York, NY). 2003; 302:1575-1577.
20. Conboy IM, Rando TA. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. DevCell. 2002; 3:397-409.
21. Walston JD. Sarcopenia in older adults. Current opinion in rheumatology. 2012; 24:623-627.
22. Sinha M, Jang YC, Oh J, Khong D, Wu EY, Manohar R, Miller C, Regalado SG, Loffredo FS, Pancoast JR, Hirshman MF, Lebowitz J, Shadrach JL, Cerletti M, Kim MJ, Serwold T, et al. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science (New York, NY). 2014; 344:649-652.
23. Modahl C, Green L, Fein D, Morris M, Waterhouse L, Feinstein C, Levin H. Plasma oxytocin levels in autistic children. Biological psychiatry. 1998; 43:270-277.
24. Ruggeri B, Sarkans U, Schumann G, Persico AM. Biomarkers in autism spectrum disorder: the old and the new. Psychopharmacology. 2014; 231:1201-1216.
25. Doyle KP, Cekanaviciute E, Mamer LE, Buckwalter MS. TGFbeta signaling in the brain increases with aging and signals to astrocytes and innate immune cells in the weeks after stroke. Journal of neuroinflammation. 2010; 7:62.
26. Allen RE, Boxhorn LK. Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. Journal of cellular physiology. 1989; 138:311-315.
27. Buckwalter MS, Yamane M, Coleman BS, Ormerod BK, Chin JT, Palmer T, Wyss-Coray T. Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am J Pathol. 2006; 169:154-164.
28. Carlson ME, Suetta C, Conboy MJ, Aagaard P, Mackey A, Kjaer M, Conboy I. Molecular aging and rejuvenation of human muscle stem cells. EMBO molecular medicine. 2009; 1:381-391.
29. Han G, Li F, Singh TP, Wolf P, Wang XJ. The proinflammatory role of TGFbeta1: a paradox?. International journal of biological sciences. 2012; 8:228-235.
30. Bohatschek M, Kloss CU, Hristova M, Pfeffer K, Raivich G. Microglial major histocompatibility complex glycoprotein-1 in the axotomized facial motor nucleus: regulation and role of tumor necrosis factor receptors 1 and 2. The Journal of comparative neurology. 2004; 470:382-399.
31. Rico MC, Rough JJ, Del Carpio-Cano FE, Kunapuli SP, DeLa Cadena RA. The axis of thrombospondin-1, transforming growth factor beta and connective tissue growth factor: an emerging therapeutic target in rheumatoid arthritis. Current vascular pharmacology. 2010; 8:338-343.
32. Sanjabi S, Zenewicz LA, Kamanaka M, Flavell RA. Anti-inflammatory and pro-inflammatory roles of TGF-beta, IL-10, and IL-22 in immunity and autoimmunity. Current opinion in pharmacology. 2009; 9:447-453.
33. Lan TH, Huang XQ, Tan HM. Vascular fibrosis in atherosclerosis. Cardiovascular pathology: the official journal of the Society for Cardiovascular Pathology. 2013; 22:401-407.
34. Carmena JM, Lebedev MA, Crist RE, O'Doherty JE, Santucci DM, Dimitrov DF, Patil PG, Henriquez CS, Nicolelis MA. Learning to control a brain-machine interface for reaching and grasping by primates. PLoS biology. 2003; 1:E42.
35. Carlson ME, Hsu M, Conboy IM. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature. 2008; 454:528-532.
36. Inman GJ. Switching TGFbeta from a tumor suppressor to a tumor promoter. Current opinion in genetics & development. 2011; 21:93-99.
37. Yoo YD, Choi JY, Lee SJ, Kim JS, Min BR, Lee YI, Kang YK. TGF-beta-induced cell-cycle arrest through the p21(WAF1/CIP1)-G1 cyclin/Cdks-p130 pathway in gastric-carcinoma cells. International journal of cancer Journal international du cancer. 1999; 83:512-517.
38. He Y, Zhang H, Yung A, Villeda SA, Jaeger PA, Olayiwola O, Fainberg N, Wyss-Coray T. ALK5-dependent TGF-beta signaling is a major determinant of late-stage adult neurogenesis. Nature neuroscience. 2014; 17:943-952.
39. Heinemann U, Kaufer D, Friedman A. Blood-brain barrier dysfunction, TGFbeta signaling, and astrocyte dysfunction in epilepsy. Glia. 2012; 60:1251-1257.
40. Harry GJ. Microglia during development and aging. Pharmacology & therapeutics. 2013; 139:313-326.
41. Pineda JR, Boussin FD, Mouthon MA. [TGFbeta, a troublemaker in the adult neural stem cell niche]. Medecine sciences: M/S. 2013; 29:572-574.
42. Gartel AL, Radhakrishnan SK. Lost in transcription: p21 repression, mechanisms, and consequences. Cancer research. 2005; 65:3980-3985.
43. Jeong J, Conboy MJ, Conboy IM. Pharmacological inhibition of myostatin/TGF-beta receptor/pSmad3 signaling rescues muscle regenerative responses in mouse model of type 1 diabetes. Acta pharmacologica Sinica. 2013; 34:1052-1060.
44. Miranda CJ, Braun L, Jiang Y, Hester ME, Zhang L, Riolo M, Wang H, Rao M, Altura RA, Kaspar BK. Aging brain microenvironment decreases hippocampal neurogenesis through Wnt-mediated survivin signaling. Aging cell. 2012; 11:542-552.
45. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annual review of neuroscience. 2005; 28:223-250.
46. Conboy IM, Rando TA. Aging, stem cells and tissue regeneration: lessons from muscle. Cell cycle (Georgetown, Tex). 2005; 4:407-410.
47. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature. 2005; 433:760-764.
48. Dumont N, Arteaga CL. A kinase-inactive type II TGFbeta receptor impairs BMP signaling in human breast cancer cells. Biochem Biophys Res Commun. 2003; 301:108-112.
49. Hanisch UK. Proteins in microglial activation-inputs and outputs by subsets. Current protein & peptide science. 2013; 14:3-15.
50. Knight JC. Genomic modulators of the immune response. Trends in genetics: TIG. 2013; 29:74-83.
51. van den Elsen PJ. Expression regulation of major histocompatibility complex class I and class II encoding genes. Frontiers in immunology. 2011; 2:48.
52. Solheim JC. Class I MHC molecules: assembly and antigen presentation. Immunological reviews. 1999; 172:11-19.
53. Neefjes JJ, Momburg F. Cell biology of antigen presentation. Current opinion in immunology. 1993; 5:27-34.
54. Breuil V, Amri EZ, Panaia-Ferrari P, Testa J, Elabd C, Albert-Sabonnadiere C, Roux CH, Ailhaud G, Dani C, Carle GF, Euller-Ziegler L. Oxytocin and bone remodelling: relationships with neuropituitary hormones, bone status and body composition. Joint, bone, spine: revue du rhumatisme. 2011; 78:611-615.
55. Barraza JA, Grewal NS, Ropacki S, Perez P, Gonzalez A, Zak PJ. Effects of a 10-day oxytocin trial in older adults on health and well-being. Experimental and clinical psychopharmacology. 2013; 21:85-92.
56. Elabd C, Cousin W, Upadhyayula P, Chen RY, Chooljian MS, Li J, Kung S, Jiang KP, Conboy IM. Oxytocin is an age-specific circulating hormone that is necessary for muscle maintenance and regeneration. Nature Communications. 2014; in press.
57. Strakova Z, Copland JA, Lolait SJ, Soloff MS. ERK2 mediates oxytocin-stimulated PGE2 synthesis. The American journal of physiology. 1998; 274:E634-641.
58. Okamoto M, Inoue K, Iwamura H, Terashima K, Soya H, Asashima M, Kuwabara T. Reduction in paracrine Wnt3 factors during aging causes impaired adult neurogenesis. FASEB J. 2011; 25:3570-3582.
59. Seib DR, Corsini NS, Ellwanger K, Plaas C, Mateos A, Pitzer C, Niehrs C, Celikel T, Martin-Villalba A. Loss of Dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell stem cell. 2013; 12:204-214.
60. Singh T, Newman AB. Inflammatory markers in population studies of aging. Ageing research reviews. 2011; 10:319-329.
61. Torchinsky MB, Blander JM. T helper 17 cells: discovery, function, and physiological trigger. Cellular and molecular life sciences: CMLS. 2010; 67:1407-1421.
62. Elabd C, Basillais A, Beaupied H, Breuil V, Wagner N, Scheideler M, Zaragosi LE, Massiera F, Lemichez E, Trajanoski Z, Carle G, Euller-Ziegler L, Ailhaud G, Benhamou CL, Dani C, Amri EZ. Oxytocin controls differentiation of human mesenchymal stem cells and reverses osteoporosis. Stem cells (Dayton, Ohio). 2008; 26:2399-2407.
63. Ashton RS, Conway A, Pangarkar C, Bergen J, Lim KI, Shah P, Bissell M, Schaffer DV. Astrocytes regulate adult hippocampal neurogenesis through ephrin-B signaling. Nature neuroscience. 2012; 15:1399-1406.
64. Babu H, Claasen JH, Kannan S, Runker AE, Palmer T, Kempermann G. A protocol for isolation and enriched monolayer cultivation of neural precursor cells from mouse dentate gyrus. Frontiers in neuroscience. 2011; 5:89.
65. Conboy MJ, Conboy IM. Preparation of adult muscle fiberassociated stem/precursor cells. Methods in molecular biology (Clifton, NJ). 2010; 621:149-163.
66. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25:402-408.
67. Peltier J, Schaffer DV. Viral packaging and transduction of adult hippocampal neural progenitors. Methods in molecular biology (Clifton, NJ). 2010; 621:103-116.
68. Yu JH, Schaffer DV. High-throughput, library-based selection of a murine leukemia virus variant to infect nondividing cells. J Virol. 2006; 80:8981-8988.
69. Conboy MJ, Cerletti M, Wagers AJ, Conboy IM. Immunoanalysis and FACS sorting of adult muscle fiber-associated stem/precursor cells. Methods in molecular biology (Clifton, NJ). 2010; 621:165-173.