Age-related changes in miR-143-3p: Igfbp5 interactions affect muscle regeneration

Aging Cell

Volumn 15, Issue 2, 2016, Pages 361-369

  Soriano Arroquia, Ana ^a   Mccormick, Rachel ^a   Molloy, Andrew P ^b   Mcardle, Anne ^a   Goljanek Whysall, Katarzyna ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY HOSPITAL AINTREE   (United Kingdom)

Author keywords

Aging; MicroRNA; Muscle; Regeneration; Sarcopenia; Senescence

Indexed keywords

INSULIN GROWTH FACTOR BINDING PROTEIN 5; INTERLEUKIN 6; MICRORNA; MICRORNA 143; MICRORNA 143 3P; PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; IGFBP5-INTERACTING PROTEIN, MOUSE; MIRN142 MICRORNA, HUMAN; MIRN143 MICRORNA, MOUSE; SOMATOMEDIN BINDING PROTEIN 5;

ADULT; AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL AGING; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALE; MOLECULAR BIOLOGY; MOUSE; MUSCLE ATROPHY; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SENESCENCE; SKELETAL MUSCLE SATELLITE CELL; VERY ELDERLY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CYTOLOGY; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE; SKELETAL MYOBLAST;

ADULT; AGED; AGING; ANIMALS; CARRIER PROTEINS; CELL AGING; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 5; MICE; MICE, INBRED C57BL; MICRORNAS; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84960082812     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12442     Document Type: Article

References (44)

1. Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, Fumagalli M, Da CM, Brown C, Popov N, Takatsu Y, Melamed J, d'Adda dFF, Bernard D, Hernando E, Gil J (2008) Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133, 1006-1018.
2. Bischoff R (1986) Proliferation of muscle satellite cells on intact myofibers in culture. Dev. Biol. 115, 129-139.
3. Blumensatt M, Wronkowitz N, Wiza C, Cramer A, Mueller H, Rabelink MJ, Hoeben RC, Eckel J, Sell H, Ouwens DM (2014) Adipocyte-derived factors impair insulin signaling in differentiated human vascular smooth muscle cells via the upregulation of miR-143. Biochim. Biophys. Acta 1842, 275-283.
4. Brack AS, Conboy MJ, Roy S, Lee M, Kuo CJ, Keller C, Rando TA (2007) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807-810.
5. Brown DM, Goljanek-Whysall K (2015) microRNAs: modulators of the underlying pathophysiology of sarcopenia? Ageing Res. Rev. 24, 267-273.
6. Carlson ME, Conboy IM (2007) Loss of stem cell regenerative capacity within aged niches. Aging Cell 6, 371-382.
7. Chen L, Wu P, Guo XH, Hu Y, Li YL, Shi J, Wang KZ, Chu WY, Zhang JS (2014) miR-143: a novel regulator of MyoD expression in fast and slow muscles of Siniperca chuatsi. Curr. Mol. Med. 14, 370-375.
8. Cheung TH, Quach NL, Charville GW, Liu L, Park L, Edalati A, Yoo B, Hoang P, Rando TA (2012) Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482, 524-528.
9. Chivukula RR, Shi G, Acharya A, Mills EW, Zeitels LR, Anandam JL, Abdelnaby AA, Balch GC, Mansour JC, Yopp AC, Maitra A, Mendell JT (2014) An essential mesenchymal function for miR-143/145 in intestinal epithelial regeneration. Cell 157, 1104-1116.
10. Cobb LJ, Salih DA, Gonzalez I, Tripathi G, Carter EJ, Lovett F, Holding C, Pell JM (2004) Partitioning of IGFBP-5 actions in myogenesis: IGF-independent anti-apoptotic function. J. Cell Sci. 117, 1737-1746.
11. Collins CA, Zammit PS, Ruiz AP, Morgan JE, Partridge TA (2007) A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells 25, 885-894.
12. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D (2009) miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460, 705-710.
13. Drummond MJ, McCarthy JJ, Fry CS, Esser KA, Rasmussen BB (2008) Aging differentially affects human skeletal muscle microRNA expression at rest and after an anabolic stimulus of resistance exercise and essential amino acids. Am. J. Physiol. Endocrinol. Metab. 295, E1333-E1340.
14. Duan C, Ren H, Gao S (2010) Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: roles in skeletal muscle growth and differentiation. Gen. Comp. Endocrinol. 167, 344-351.
15. Elia L, Quintavalle M, Zhang J, Contu R, Cossu L, Latronico MV, Peterson KL, Indolfi C, Catalucci D, Chen J, Courtneidge SA, Condorelli G (2009) The knockout of miR-143 and -145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ. 16, 1590-1598.
16. Ershler WB, Sun WH, Binkley N, Gravenstein S, Volk MJ, Kamoske G, Klopp RG, Roecker EB, Daynes RA, Weindruch R (1993) Interleukin-6 and aging: blood levels and mononuclear cell production increase with advancing age and in ;vitro production is modifiable by dietary restriction. Lymphokine Cytokine Res. 12, 225-230.
17. Esau C, Kang X, Peralta E, Hanson E, Marcusson EG, Ravichandran LV, Sun Y, Koo S, Perera RJ, Jain R, Dean NM, Freier SM, Bennett CF, Lollo B, Griffey R (2004) MicroRNA-143 regulates adipocyte differentiation. J. Biol. Chem. 279, 52361-52365.
18. Giresi PG, Stevenson EJ, Theilhaber J, Koncarevic A, Parkington J, Fielding RA, Kandarian SC (2005) Identification of a molecular signature of sarcopenia. Physiol. Genomics 21, 253-263.
19. Goljanek-Whysall K, Sweetman D, Abu-Elmagd M, Chapnik E, Dalmay T, Hornstein E, Munsterberg A (2011) MicroRNA regulation of the paired-box transcription factor Pax3 confers robustness to developmental timing of myogenesis. Proc. Natl Acad. Sci. USA 108, 11936-11941.
20. Goljanek-Whysall K, Pais H, Rathjen T, Sweetman D, Dalmay T, Munsterberg A (2012a) Regulation of multiple target genes by miR-1 and miR-206 is pivotal for C2C12 myoblast differentiation. J. Cell Sci. 125, 3590-3600.
21. Goljanek-Whysall K, Sweetman D, Munsterberg AE (2012b) microRNAs in skeletal muscle differentiation and disease. Clin. Sci. 123, 611-625.
22. Goljanek-Whysall K, Mok GF, Fahad Alrefaei A, Kennerley N, Wheeler GN, Munsterberg A (2014) myomiR-dependent switching of BAF60 variant incorporation into Brg1 chromatin remodeling complexes during embryo myogenesis. Development 141, 3378-3387.
23. Jackson MJ, McArdle A (2011) Age-related changes in skeletal muscle reactive oxygen species generation and adaptive responses to reactive oxygen species. J. Physiol. 589, 2139-2145.
24. James PL, Stewart CE, Rotwein P (1996) Insulin-like growth factor binding protein-5 modulates muscle differentiation through an insulin-like growth factor-dependent mechanism. J. Cell Biol. 133, 683-693.
25. Jejurikar SS, Henkelman EA, Cederna PS, Marcelo CL, Urbanchek MG, Kuzon WM Jr (2006) Aging increases the susceptibility of skeletal muscle derived satellite cells to apoptosis. Exp. Gerontol. 41, 828-836.
26. Jordan SD, Kruger M, Willmes DM, Redemann N, Wunderlich FT, Bronneke HS, Merkwirth C, Kashkar H, Olkkonen VM, Bottger T, Braun T, Seibler J, Bruning JC (2011) Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat. Cell Biol. 13, 434-446.
27. Kim KS, Seu YB, Baek SH, Kim MJ, Kim KJ, Kim JH, Kim JR (2007) Induction of cellular senescence by insulin-like growth factor binding protein-5 through a p53-dependent mechanism. Mol. Biol. Cell 18, 4543-4552.
28. Kim JY, Park YK, Lee KP, Lee SM, Kang TW, Kim HJ, Dho SH, Kim SY, Kwon KS (2014) Genome-wide profiling of the microRNA-mRNA regulatory network in skeletal muscle with aging. Aging 6, 524-544.
29. Kojima H, Inoue T, Kunimoto H, Nakajima K (2013) IL-6-STAT3 signaling and premature senescence. Jak-Stat 2, e25763.
30. McCarthy JJ, Esser KA (2007) MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J. Appl. Physiol. 102, 306-313.
31. Morgan JE, Partridge TA (2003) Muscle satellite cells. Int. J. Biochem. Cell Biol. 35, 1151-1156.
32. Pasut A, Jones AE, Rudnicki MA (2013) Isolation and culture of individual myofibers and their satellite cells from adult skeletal muscle. J. Vis. Exp., 73, e50074. doi:10.3791/50074.
33. Ren H, Yin P, Duan C (2008) IGFBP-5 regulates muscle cell differentiation by binding to IGF-II and switching on the IGF-II auto-regulation loop. J. Cell Biol. 182, 979-991.
34. Salih DA, Tripathi G, Holding C, Szestak TA, Gonzalez MI, Carter EJ, Cobb LJ, Eisemann JE, Pell JM (2004) Insulin-like growth factor-binding protein 5 (Igfbp5) compromises survival, growth, muscle development, and fertility in mice. Proc. Natl Acad. Sci. USA 101, 4314-4319.
35. Soares RJ, Cagnin S, Chemello F, Silvestrin M, Musaro A, De Pitta C, Lanfranchi G, Sandri M (2014) Involvement of microRNAs in the regulation of muscle wasting during catabolic conditions. J. Biol. Chem. 289, 21909-21925.
36. Sousa-Victor P, Gutarra S, Garcia-Prat L, Rodriguez-Ubreva J, Ortet L, Ruiz-Bonilla V, Jardi M, Ballestar E, Gonzalez S, Serrano AL, Perdiguero E, Munoz-Canoves P (2014) Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 506, 316-321.
37. Sreekumar R, Halvatsiotis P, Schimke JC, Nair KS (2002) Gene expression profile in skeletal muscle of type 2 diabetes and the effect of insulin treatment. Diabetes 51, 1913-1920.
38. Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HH, van Loon LJ (2007) Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am. J. Physiol. Endocrinol. Metab. 292, E151-E157.
39. Wang HV, Chang LW, Brixius K, Wickstrom SA, Montanez E, Thievessen I, Schwander M, Muller U, Bloch W, Mayer U, Fassler R (2008) Integrin-linked kinase stabilizes myotendinous junctions and protects muscle from stress-induced damage. J. Cell Biol. 180, 1037-1049.
40. Washington TA, White JP, Davis JM, Wilson LB, Lowe LL, Sato S, Carson JA (2011) Skeletal muscle mass recovery from atrophy in IL-6 knockout mice. Acta Physiol. 202, 657-669.
41. Williams AH, Valdez G, Moresi V, Qi X, McAnally J, Elliott JL, Bassel-Duby R, Sanes JR, Olson EN (2009) MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 326, 1549-1554.
42. Xin M, Small EM, Sutherland LB, Qi X, McAnally J, Plato CF, Richardson JA, Bassel-Duby R, Olson EN (2009) MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev. 23, 2166-2178.
43. Yi L, Rossi F (2011) Purification of progenitors from skeletal muscle. J. Vis. Exp. 49, e2476. doi:10.3791/2476.
44. Zhang D, Li X, Chen C, Li Y, Zhao L, Jing Y, Liu W, Wang X, Zhang Y, Xia H, Chang Y, Gao X, Yan J, Ying H (2012) Attenuation of p38-mediated miR-1/133 expression facilitates myoblast proliferation during the early stage of muscle regeneration. PLoS ONE 7, e41478.