Lkb1 is indispensable for skeletal muscle development, regeneration, and satellite cell homeostasis

Stem Cells

Volumn 32, Issue 11, 2014, Pages 2893-2907

  Shan, Tizhong ^a   Zhang, Pengpeng ^a   Liang, Xinrong ^a   Bi, Pengpeng ^a   Yue, Feng ^a   Kuang, Shihuan ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Liver kinase b1; Myogenesis; Serine threonine kinase 11; Stem cells

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; PROTEIN SERINE THREONINE KINASE; STK11 PROTEIN, MOUSE;

ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; HOMEOSTASIS; LIVER; METABOLISM; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE CELL; SKELETAL MUSCLE SATELLITE CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; GLYCOGEN SYNTHASE KINASE 3; HOMEOSTASIS; LIVER; MICE; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MYOBLASTS; PROTEIN-SERINE-THREONINE KINASES; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84907899129     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1788     Document Type: Article

References (79)

1. Sambasivan R, Yao R, Kissenpfennig A, et al. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 2011; 138: 3647-3656.
2. Lepper C, Partridge TA, Fan CM,. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 2011; 138: 3639-3646.
3. Murphy MM, Lawson JA, Mathew SJ, et al. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 2011; 138: 3625-3637.
4. Collins CA, Olsen I, Zammit PS, et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 2005; 122: 289-301.
5. Montarras D, Morgan J, Collins C, et al. Direct isolation of satellite cells for skeletal muscle regeneration. Science 2005; 309: 2064-2067.
6. Kuang S, Kuroda K, Le Grand F, et al. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 2007; 129: 999-1010.
7. Wang YX, Rudnicki MA,. Satellite cells, the engines of muscle repair. Nat Rev Mol Cell Biol 2012; 13: 127-133.
8. Brack AS, Rando TA,. Tissue-specific stem cells: Lessons from the skeletal muscle satellite cell. Cell Stem Cell 2012; 10: 504-514.
9. Kuang S, Rudnicki MA,. The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 2008; 14: 82-91.
10. Zammit PS, Golding JP, Nagata Y, et al. Muscle satellite cells adopt divergent fates: A mechanism for self-renewal? J Cell Biol 2004; 166: 347-357.
11. Olguin HC, Olwin BB,. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: A potential mechanism for self-renewal. Dev Biol 2004; 275: 375-388.
12. Halevy O, Piestun Y, Allouh MZ, et al. Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 2004; 231: 489-502.
13. Wen Y, Bi P, Liu W, et al. Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol Cell Biol 2012; 32: 2300-2311.
14. Kuang S, Gillespie MA, Rudnicki MA,. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2008; 2: 22-31.
15. Conboy IM, Rando TA,. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 2002; 3: 397-409.
16. Bjornson CRR, Cheung TH, Liu L, et al. Notch Signaling Is Necessary to Maintain Quiescence in Adult Muscle Stem Cells. Stem Cells 2012; 30: 232-242.
17. Mourikis P, Sambasivan R, Castel D, et al. A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 2012; 30: 243-252.
18. Brack AS, Conboy MJ, Roy S, et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007; 317: 807-810.
19. von Maltzahn J, Chang NC, Bentzinger CF, et al. Wnt signaling in myogenesis. Trends Cell Biol 2012; 22: 602-609.
20. Serrano AL, Baeza-Raja B, Perdiguero E, et al. Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 2008; 7: 33-44.
21. Musaro A, Giacinti C, Borsellino G, et al. Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proc Natl Acad Sci USA 2004; 101: 1206-1210.
22. Rocheteau P, Gayraud-Morel B, Siegl-Cachedenier I, et al. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 2012; 148: 112-125.
23. Montarras D, L'honore A, Buckingham M,. Lying low but ready for action: The quiescent muscle satellite cell. FEBS J 2013; 280: 4036-4050.
24. Cheung TH, Quach NL, Charville GW, et al. Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 2012; 482: 524-U247.
25. Hemminki A, Markie D, Tomlinson I, et al. A serine/threonine kinase gene defective in Peutz-Jegheus syndrome. Nature 1998; 391: 184-187.
26. Jenne DE, Reimann H, Nezu J, et al. Peutz-Jeghers syndrome is caused by mutations in a novel serine threonine kinase. Nat Genet 1998; 18: 38-44.
27. Ji H, Ramsey MR, Hayes DN, et al. LKB1 modulates lung cancer differentiation and metastasis. Nature 2007; 448: 807-810.
28. Gao Y, Xiao Q, Ma H, et al. LKB1 inhibits lung cancer progression through lysyl oxidase and extracellular matrix remodeling. Proc Natl Acad Sci USA 2010; 107: 18892-18897.
29. Hardie DG,. The LKB1-AMPK pathway-friend or foe in cancer? Cancer Cell 2013; 23: 131-132.
30. Mirouse V, Swick LL, Kazgan N, et al. LKB1 and AMPK maintain epithelial cell polarity under energetic stress. J Cell Biol 2007; 177: 387-392.
31. Amin N, Khan A, St Johnston D, et al. LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye. Proc Natl Acad Sci USA 2009; 106: 8941-8946.
32. Granot Z, Swisa A, Magenheim J, et al. LKB1 regulates pancreatic beta cell size, polarity, and function. Cell Metab 2009; 10: 296-308.
33. Zagorska A, Deak M, Campbell DG, et al. New roles for the LKB1-NUAK pathway in controlling myosin phosphatase complexes and cell Adhesion. Sci Signal 2010; 3.
34. Karuman P, Gozani O, Odze RD, et al. The Peutz-Jegher gene product LKB1 is a mediator of p53-dependent cell death. Mol Cell 2001; 7: 1307-1319.
35. Nakada D, Saunders TL, Morrison SJ,. Lkb1 regulates cell cycle and energy metabolism in haematopoietic stem cells. Nature 2010; 468: 653-U669.
36. Bonaccorsi S, Mottier V, Giansanti MG, et al. The Drosophila Lkb1 kinase is required for spindle formation and asymmetric neuroblast division. Development 2007; 134: 2183-2193.
37. Denning DP, Hatch V, Horvitz HR,. Programmed elimination of cells by caspase-independent cell extrusion in C. elegans. Nature 2012; 488: 226-230.
38. Fu A, Ng ACH, Depatie C, et al. Loss of Lkb1 in adult beta cells increases beta cell mass and enhances glucose tolerance in mice. Cell Metab 2009; 10: 285-295.
39. Tamas P, Macintyre A, Finlay D, et al. LKB1 is essential for the proliferation of T-cell progenitors and mature peripheral T cells. Eur J Immunol 2010; 40: 242-253.
40. Lai LP, Lilley BN, Sanes JR, et al. Lkb1/Stk11 regulation of mTOR signaling controls the transition of chondrocyte fates and suppresses skeletal tumor formation. Proc Natl Acad Sci USA 2013; 110: 19450-19455.
41. Krock B, Skuli N, Simon MC,. The tumor suppressor LKB1 emerges as a critical factor in hematopoietic stem cell biology. Cell Metab 2011; 13: 8-10.
42. Gurumurthy S, Xie SZ, Alagesan B, et al. The Lkb1 metabolic sensor maintains haematopoietic stem cell survival. Nature 2010; 468: 659-U675.
43. Gan BY, Hu JA, Jiang S, et al. Lkb1 regulates quiescence and metabolic homeostasis of haematopoietic stem cells. Nature 2010; 468: 701-U125.
44. Lai D, Chen Y, Wang F, et al. LKB1 controls the pluripotent state of human embryonic stem cells. Cell Reprogram 2012; 14: 164-170.
45. Durand EM, Zon LI,. The blood balance. Nature 2010; 468: 644-645.
46. David R,. LKB1 maintains the balance. Nat Rev Mol Cell Biol 2011; 12.
47. Lizcano JM, Goransson O, Toth R, et al. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J 2004; 23: 833-843.
48. Ylikorkala A, Rossi DJ, Korsisaari N, et al. Vascular abnormalities and deregulation of VEGF in Lkb1-deficient mice. Science 2001; 293: 1323-1326.
49. Koh HJ, Arnolds DE, Fujii N, et al. Skeletal muscle-selective knockout of LKB1 increases insulin sensitivity, improves, glucose homeostasis, and decreases TRB3. Mol Cell Biol 2006; 26: 8217-8227.
50. Thomson DM, Hancock CR, Evanson BG, et al. Skeletal muscle dysfunction in muscle-specific LKB1 knockout mice. J Appl Physiol 2010; 108: 1775-1785.
51. Jeppesen J, Maarbjerg SJ, Jordy AB, et al. LKB1 regulates lipid oxidation during exercise independently of AMPK. Diabetes 2013; 62: 1490-1499.
52. Shan TZ, Liang XR, Bi PP, et al. Myostatin knockout drives browning of white adipose tissue through activating the AMPK-PGC1 alpha-Fndc5 pathway in muscle. FASEB J 2013; 27: 1981-1989.
53. Shan T, Liang X, Bi P, et al. Distinct populations of adipogenic and myogenic Myf5-lineage progenitors in white adipose tissues. J Lipid Res 2013; 54: 2214-2224.
54. Bondesen BA, Jones KA, Glasgow WC, et al. Inhibition of myoblast migration by prostacyclin is associated with enhanced cell fusion. FASEB J 2007; 21: 3338-3345.
55. Yoshida N, Yoshida S, Koishi K, et al. Cell heterogeneity upon myogenic differentiation: Down-regulation of MyoD and Myf-5 generates 'reserve cells'. J Cell Sci 1998; 111: 769-779.
56. Shan TZ, Liu WY, Kuang SH,. Fatty acid binding protein 4 expression marks a population of adipocyte progenitors in white and brown adipose tissues. FASEB J 2013; 27: 277-287.
57. Meinen S, Barzaghi P, Lin S, et al. Linker molecules between laminins and dystroglycan ameliorate laminin-α2-deficient muscular dystrophy at all disease stages. J Cell Biol 2007; 176: 979-993.
58. Luukko K, Ylikorkala A, Tiainen M, et al. Expression of LKB1 and PTEN tumor suppressor genes during mouse embryonic development. Mech Dev 1999; 83: 187-190.
59. Kanisicak O, Mendez JJ, Yamamoto S, et al. Progenitors of skeletal muscle satellite cells express the muscle determination gene, MyoD. Dev Biol 2009; 332: 131-141.
60. Liu W, Wen Y, Bi P, et al. Hypoxia promotes satellite cell self-renewal and enhances the efficiency of myoblast transplantation. Development 2012; 139: 2857-2865.
61. Ossipova O, Bardeesy N, DePinho RA, et al. LKB1 (XEEK1) regulates Wnt signalling in vertebrate development. Nat Cell Biol 2003; 5: 889-894.
62. Asada N, Sanada K,. LKB1-mediated spatial control of GSK3 beta and adenomatous polyposis coli contributes to centrosomal forward movement and neuronal migration in the developing neocortex. J Neurosci 2010; 30: 8852-8865.
63. Tanner CB, Madsen SR, Hallowell DM, et al. Mitochondrial and performance adaptations to exercise training in mice lacking skeletal muscle LKB1. Am J Physiol Endocrinol Metab 2013; 305: E1018-1029.
64. Miura S, Kai Y, Tadaishi M, et al. Marked phenotypic differences of endurance performance and exercise-induced oxygen consumption between AMPK and LKB1 deficiency in mouse skeletal muscle: Changes occurring in the diaphragm. Am J Physiol Endocrinol Metab 2013; 305: E213-E229.
65. Thomson M, Porter BB, Tall JH, et al. Skeletal muscle and heart LKB1 deficiency causes decreased voluntary running and reduced muscle mitochondrial marker enzyme expression in mice. Am J Physiol Endocrinol Metab 2007; 292: E196-E202.
66. Sakamoto K, McCarthy A, Smith D, et al. Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction. EMBO J 2005; 24: 1810-1820.
67. Wood WM, Etemad S, Yamamoto M, et al. MyoD-expressing progenitors are essential for skeletal myogenesis and satellite cell development. Dev Biol 2013; 384: 114-127.
68. Lin J, Wu H, Tarr PT, et al. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature 2002; 418: 797-801.
69. Gerhart-Hines Z, Rodgers JT, Bare O, et al. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1α. EMBO J 2007; 26: 1913-1923.
70. Risson V, Mazelin L, Roceri M, et al. Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J Cell Biol 2009; 187: 859-874.
71. Bentzinger CF, Romanino K, Cloetta D, et al. Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab 2008; 8: 411-424.
72. Thomson DM, Brown JD, Fillmore N, et al. LKB1 and the regulation of malonyl-CoA and fatty acid oxidation in muscle. Am J Physiol Endocrinol Metab 2007; 293: E1572-E1579.
73. Berdeaux R, Goebel N, Banaszynski L, et al. SIK1 is a class IIHDAC kinase that promotes survival of skeletal myocytes. Nat Med 2007; 13: 597-603.
74. Stewart R, Akhmedov D, Robb C, et al. Regulation of SIK1 abundance and stability is critical for myogenesis. Proc Natl Acad Sci USA 2013; 110: 117-122.
75. McKinsey TA, Zhang CL, Lu JR, et al. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 2000; 408: 106-111.
76. Katajisto P, Vaahtomeri K, Ekman N, et al. LKB1 signaling in mesenchymal cells required for suppression of gastrointestinal polyposis. Nat Genet 2008; 40: 455-459.
77. Lo B, Strasser G, Sagolla M, et al. Lkb1 regulates organogenesis and early oncogenesis along AMPK-dependent and -independent pathways. J Cell Biol 2012; 199: 1117-1130.
78. Hezel AF, Gurumurthy S, Granot Z, et al. Pancreatic Lkb1 deletion leads to acinar polarity defects and cystic neoplasms. Mol Cell Biol 2008; 28: 2414-2425.
79. Brack AS, Conboy IM, Conboy MJ, et al. A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2008; 2: 50-59.