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Roles of leptin in the recovery of muscle and bone by reloading after mechanical unloading in high fat diet-fed obese mice


Autoři: Naoyuki Kawao aff001;  Masayoshi Ishida aff001;  Hiroshi Kaji aff001
Působiště autorů: Department of Physiology and Regenerative Medicine, Kindai University Faculty of Medicine, Osakasayama, Japan aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224403

Souhrn

Muscle and bone masses are elevated by the increased mechanical stress associated with body weight gain in obesity. However, the mechanisms by which obesity affects muscle and bone remain unclear. We herein investigated the roles of obesity and humoral factors from adipose tissue in the recovery phase after reloading from disuse-induced muscle wasting and bone loss using normal diet (ND)- or high fat diet (HFD)-fed mice with hindlimb unloading (HU) and subsequent reloading. Obesity did not affect decreases in trabecular bone mineral density (BMD), muscle mass in the lower leg, or grip strength in HU mice. Obesity significantly increased trabecular BMD, muscle mass in the lower leg, and grip strength in reloading mice over those in reloading mice fed ND. Among the humoral factors in epididymal and subcutaneous adipose tissue, leptin mRNA levels were significantly higher in reloading mice fed HFD than in mice fed ND. Moreover, circulating leptin levels were significantly higher in reloading mice fed HFD than in mice fed ND. Leptin mRNA levels in epididymal adipose tissue or serum leptin levels positively correlated with the increases in trabecular BMD, total muscle mass, and grip strength in reloading mice fed ND and HFD. The present study is the first to demonstrate that obesity enhances the recovery of bone and muscle masses as well as strength decreased by disuse after reloading in mice. Leptin may contribute to the recovery of muscle and bone enhanced by obesity in mice.

Klíčová slova:

Adipose tissue – Body weight – Fats – Legs – leptin – Obesity – Skeletal muscles


Zdroje

1. Savvidis C, Tournis S, Dede AD. Obesity and bone metabolism. Hormones (Athens). 2018;17: 205–217.

2. Batsis JA, Villareal DT. Sarcopenic obesity in older adults: aetiology, epidemiology and treatment strategies. Nat Rev Endocrinol. 2018;14: 513–537. doi: 10.1038/s41574-018-0062-9 30065268

3. Tallis J, Hill C, James RS, Cox VM, Seebacher F. The effect of obesity on the contractile performance of isolated mouse soleus, EDL, and diaphragm muscles. J Appl Physiol (1985). 2017;122: 170–181.

4. Evans AL, Paggiosi MA, Eastell R, Walsh JS. Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J Bone Miner Res. 2015;30: 920–928. doi: 10.1002/jbmr.2407 25400253

5. De Laet C, Kanis JA, Oden A, Johanson H, Johnell O, Delmas P, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int. 2005;16: 1330–1338. doi: 10.1007/s00198-005-1863-y 15928804

6. Compston JE, Watts NB, Chapurlat R, Cooper C, Boonen S, Greenspan S, et al. Obesity is not protective against fracture in postmenopausal women: GLOW. Am J Med. 2011;124: 1043–1050. doi: 10.1016/j.amjmed.2011.06.013 22017783

7. Lecka-Czernik B, Stechschulte LA, Czernik PJ, Dowling AR. High bone mass in adult mice with diet-induced obesity results from a combination of initial increase in bone mass followed by attenuation in bone formation; implications for high bone mass and decreased bone quality in obesity. Mol Cell Endocrinol. 2015;410: 35–41. doi: 10.1016/j.mce.2015.01.001 25576855

8. Viljakainen H, Ivaska KK, Paldanius P, Lipsanen-Nyman M, Saukkonen T, Pietilainen KH, et al. Suppressed bone turnover in obesity: a link to energy metabolism? A case-control study. J Clin Endocrinol Metab. 2014;99: 2155–2163. doi: 10.1210/jc.2013-3097 24606073

9. Garcia-Vicencio S, Coudeyre E, Kluka V, Cardenoux C, Jegu AG, Fourot AV, et al. The bigger, the stronger? Insights from muscle architecture and nervous characteristics in obese adolescent girls. Int J Obes (Lond). 2016;40: 245–251.

10. Wang X, Zhao D, Cui Y, Lu S, Gao D, Liu J. Proinflammatory macrophages impair skeletal muscle differentiation in obesity through secretion of tumor necrosis factor-alpha via sustained activation of p38 mitogen-activated protein kinase. J Cell Physiol. 2019;234: 2566–2580. doi: 10.1002/jcp.27012 30264458

11. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol. 2006;6: 772–783. doi: 10.1038/nri1937 16998510

12. Tamura Y, Kawao N, Shimoide T, Okada K, Matsuo O, Kaji H. Role of plasminogen activator inhibitor-1 in glucocorticoid-induced muscle change in mice. J Bone Miner Metab. 2018;36: 148–156. doi: 10.1007/s00774-017-0825-8 28321652

13. Roy B, Curtis ME, Fears LS, Nahashon SN, Fentress HM. Molecular mechanisms of obesity-induced osteoporosis and muscle atrophy. Front Physiol. 2016;7: 439. doi: 10.3389/fphys.2016.00439 27746742

14. Kaji H. Adipose tissue-derived plasminogen activator inhibitor-1 function and regulation. Compr Physiol. 2016;6: 1873–1896. doi: 10.1002/cphy.c160004 27783862

15. Naot D, Musson DS, Cornish J. The activity of adiponectin in bone. Calcif Tissue Int. 2017;100: 486–499. doi: 10.1007/s00223-016-0216-5 27928591

16. Richards JB, Valdes AM, Burling K, Perks UC, Spector TD. Serum adiponectin and bone mineral density in women. J Clin Endocrinol Metab. 2007;92: 1517–1523. doi: 10.1210/jc.2006-2097 17264180

17. Chen XX, Yang T. Roles of leptin in bone metabolism and bone diseases. J Bone Miner Metab. 2015;33: 474–485. doi: 10.1007/s00774-014-0569-7 25777984

18. Bartell SM, Rayalam S, Ambati S, Gaddam DR, Hartzell DL, Hamrick M, et al. Central (ICV) leptin injection increases bone formation, bone mineral density, muscle mass, serum IGF-1, and the expression of osteogenic genes in leptin-deficient ob/ob mice. J Bone Miner Res. 2011;26: 1710–1720. doi: 10.1002/jbmr.406 21520275

19. Philbrick KA, Martin SA, Colagiovanni AR, Branscum AJ, Turner RT, Iwaniec UT. Effects of hypothalamic leptin gene therapy on osteopetrosis in leptin-deficient mice. J Endocrinol. 2018;236: 57–68. doi: 10.1530/JOE-17-0524 29191939

20. Kalra SP, Dube MG, Iwaniec UT. Leptin increases osteoblast-specific osteocalcin release through a hypothalamic relay. Peptides. 2009;30: 967–973. doi: 10.1016/j.peptides.2009.01.020 19428775

21. Hamrick MW. Role of the cytokine-like hormone leptin in muscle-bone crosstalk with aging. J Bone Metab. 2017;24: 1–8. doi: 10.11005/jbm.2017.24.1.1 28326295

22. Kawao N, Kaji H. Interactions between muscle tissues and bone metabolism. J Cell Biochem. 2015;116: 687–695. doi: 10.1002/jcb.25040 25521430

23. Stein TP. Weight, muscle and bone loss during space flight: another perspective. Eur J Appl Physiol. 2013;113: 2171–2181. doi: 10.1007/s00421-012-2548-9 23192310

24. Kawao N, Moritake A, Tatsumi K, Kaji H. Roles of irisin in the linkage from muscle to bone during mechanical unloading in mice. Calcif Tissue Int. 2018;103: 24–34. doi: 10.1007/s00223-018-0387-3 29332162

25. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010;25: 1468–1486. doi: 10.1002/jbmr.141 20533309

26. Ravussin Y, Edwin E, Gallop M, Xu L, Bartolome A, Kraakman MJ, et al. Evidence for a non-leptin system that defends against weight gain in overfeeding. Cell Metab. 2018;28: 289–299 e285. doi: 10.1016/j.cmet.2018.05.029 29937378

27. Tamura Y, Kawao N, Yano M, Okada K, Okumoto K, Chiba Y, et al. Role of plasminogen activator inhibitor-1 in glucocorticoid-induced diabetes and osteopenia in mice. Diabetes. 2015;64: 2194–2206. doi: 10.2337/db14-1192 25552599

28. Lee NJ, Ali N, Zhang L, Qi Y, Clarke I, Enriquez RF, et al. Osteoglycin, a novel coordinator of bone and glucose homeostasis. Mol Metab. 2018;13: 30–44. doi: 10.1016/j.molmet.2018.05.004 29799418

29. Ke HZ, Richards WG, Li X, Ominsky MS. Sclerostin and Dickkopf-1 as therapeutic targets in bone diseases. Endocr Rev. 2012;33: 747–783. doi: 10.1210/er.2011-1060 22723594

30. Keune JA, Branscum AJ, Wong CP, Iwaniec UT, Turner RT. Effect of leptin deficiency on the skeletal response to hindlimb unloading in adult male mice. Sci Rep. 2019;9: 9336. doi: 10.1038/s41598-019-45587-0 31249331

31. Westerlind KC, Fluckey JD, Gordon SE, Kraemer WJ, Farrell PA, Turner RT. Effect of resistance exercise training on cortical and cancellous bone in mature male rats. J Appl Physiol (1985). 1998;84: 459–464.

32. Tromp AM, Bravenboer N, Tanck E, Oostlander A, Holzmann PJ, Kostense PJ, et al. Additional weight bearing during exercise and estrogen in the rat: the effect on bone mass, turnover, and structure. Calcif Tissue Int. 2006;79: 404–415. doi: 10.1007/s00223-006-0045-z 17160577

33. Song H, Cho S, Lee HY, Lee H, Song W. The effects of progressive resistance exercise on recovery rate of bone and muscle in a rodent model of hindlimb suspension. Front Physiol. 2018;9: 1085. doi: 10.3389/fphys.2018.01085 30150940

34. Banzrai C, Nodera H, Kawarai T, Higashi S, Okada R, Mori A, et al. Impaired axonal Na+ current by hindlimb unloading: implication for disuse neuromuscular atrophy. Front Physiol. 2016;7: 36. doi: 10.3389/fphys.2016.00036 26909041

35. Avraham Y, Davidi N, Lassri V, Vorobiev L, Kabesa M, Dayan M, et al. Leptin induces neuroprotection neurogenesis and angiogenesis after stroke. Curr Neurovasc Res. 2011;8: 313–322. 22023616

36. Turner RT, Kalra SP, Wong CP, Philbrick KA, Lindenmaier LB, Boghossian S, et al. Peripheral leptin regulates bone formation. J Bone Miner Res. 2013;28: 22–34. doi: 10.1002/jbmr.1734 22887758

37. Gordeladze JO, Drevon CA, Syversen U, Reseland JE. Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: Impact on differentiation markers, apoptosis, and osteoclastic signaling. J Cell Biochem. 2002;85: 825–836. doi: 10.1002/jcb.10156 11968022

38. Holloway WR, Collier FM, Aitken CJ, Myers DE, Hodge JM, Malakellis M, et al. Leptin inhibits osteoclast generation. J Bone Miner Res. 2002;17: 200–209. doi: 10.1359/jbmr.2002.17.2.200 11811550

39. Yamauchi M, Sugimoto T, Yamaguchi T, Nakaoka D, Kanzawa M, Yano S, et al. Plasma leptin concentrations are associated with bone mineral density and the presence of vertebral fractures in postmenopausal women. Clin Endocrinol (Oxf). 2001;55: 341–347.

40. Roux C, Arabi A, Porcher R, Garnero P. Serum leptin as a determinant of bone resorption in healthy postmenopausal women. Bone. 2003;33: 847–852. doi: 10.1016/j.bone.2003.07.008 14623061

41. Arounleut P, Bowser M, Upadhyay S, Shi XM, Fulzele S, Johnson MH, et al. Absence of functional leptin receptor isoforms in the POUND (Leprdb/lb) mouse is associated with muscle atrophy and altered myoblast proliferation and differentiation. PLoS One. 2013;8: e72330. doi: 10.1371/journal.pone.0072330 23967295

42. Sainz N, Rodriguez A, Catalan V, Becerril S, Ramirez B, Gomez-Ambrosi J, et al. Leptin administration favors muscle mass accretion by decreasing FoxO3a and increasing PGC-1α in ob/ob mice. PLoS One. 2009;4: e6808. doi: 10.1371/journal.pone.0006808 19730740

43. McNelis JC, Olefsky JM. Macrophages, immunity, and metabolic disease. Immunity. 2014;41: 36–48. doi: 10.1016/j.immuni.2014.05.010 25035952

44. Lim JP, Leung BP, Ding YY, Tay L, Ismail NH, Yeo A, et al. Monocyte chemoattractant protein-1: a proinflammatory cytokine elevated in sarcopenic obesity. Clin Interv Aging. 2015;10: 605–609. doi: 10.2147/CIA.S78901 25848236

45. Koh TJ, Bryer SC, Pucci AM, Sisson TH. Mice deficient in plasminogen activator inhibitor-1 have improved skeletal muscle regeneration. Am J Physiol Cell Physiol. 2005;289: C217–223. doi: 10.1152/ajpcell.00555.2004 15716324

46. Freire PP, Cury SS, de Oliveira G, Fernandez GJ, Moraes LN, da Silva Duran BO, et al. Osteoglycin inhibition by microRNA miR-155 impairs myogenesis. PLoS One. 2017;12: e0188464. doi: 10.1371/journal.pone.0188464 29161332

47. Fruhbeck G, Mendez-Gimenez L, Fernandez-Formoso JA, Fernandez S, Rodriguez A. Regulation of adipocyte lipolysis. Nutr Res Rev. 2014;27: 63–93. doi: 10.1017/S095442241400002X 24872083

48. Kondo H, Nifuji A, Takeda S, Ezura Y, Rittling SR, Denhardt DT, et al. Unloading induces osteoblastic cell suppression and osteoclastic cell activation to lead to bone loss via sympathetic nervous system. J Biol Chem. 2005;280: 30192–30200. doi: 10.1074/jbc.M504179200 15961387

49. Hariri N, Thibault L. High-fat diet-induced obesity in animal models. Nutr Res Rev. 2010;23: 270–299. doi: 10.1017/S0954422410000168 20977819

50. Fuchs T, Loureiro MP, Macedo LE, Nocca D, Nedelcu M, Costa-Casagrande TA. Animal models in metabolic syndrome. Rev Col Bras Cir. 2018;45: e1975. doi: 10.1590/0100-6991e-20181975 30379216

51. Cauley JA. An overview of sarcopenic obesity. J Clin Densitom. 2015;18: 499–505. doi: 10.1016/j.jocd.2015.04.013 26141163

52. Polyzos SA, Margioris AN. Sarcopenic obesity. Hormones (Athens). 2018;17: 321–331.


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