Sex-specific autophagy modulation in osteoblastic lineage: A critical function to counteract bone loss in female

Oncotarget

Volumn 7, Issue 41, 2016, Pages 66416-66428

  Camuzard, Olivier ^a,b   Santucci Darmanin, Sabine ^a   Breuil, Véronique ^a,b   Cros, Chantal ^a   Gritsaenko, Tatiana ^a   Pagnotta, Sophie ^c   Cailleteau, Laurence ^b   Battaglia, Séverine ^d   Panaïa Ferrari, Patricia ^b   Heymann, Dominique ^d,e   Carle, Georges F ^a   Pierrefite Carle, Valérie ^a  

^a Laboratoire TIRO   (France)

^b UNIVERSITY HOSPITAL OF NICE   (France)

^c Universite Co te d'Azur Parc Valrose   (France)

^d Universite de Nantes   (France)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Aging; Autophagy; Gerotarget; Osteoblast; Osteocyte; Osteoporosis

Indexed keywords

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL ACTIVITY; CELL LINEAGE; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GONADECTOMY; HORMONE RESPONSE; MALE; MOUSE; MOUSE MODEL; NONHUMAN; ORCHIECTOMY; OSTEOBLAST; OSTEOCYTE; OSTEOLYSIS; OVARIECTOMY; OXIDATIVE STRESS; SEX DIFFERENCE; ANIMAL; OSTEOPOROSIS; PATHOLOGY; PHYSIOLOGY; SEXUAL CHARACTERISTICS;

ANIMALS; AUTOPHAGY; FEMALE; MALE; MICE; OSTEOBLASTS; OSTEOCYTES; OSTEOPOROSIS; SEX CHARACTERISTICS;

EID: 84993949487     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12013     Document Type: Article

References (50)

1. Raggatt LJ, Partridge NC. Cellular and molecular mechanisms of bone remodeling. Journal of Biological Chemistry. 2010; 285: 25103-25108.
2. Kular J, Tickner J, Chim SM, Xu J. An overview of the regulation of bone remodelling at the cellular level. Clinical Biochemistry. 2012; 45: 863-873.
3. Hendrickx G, Boudin E, Van Hul W. A look behind the scenes: the risk and pathogenesis of primary osteoporosis. Nature Reviews Rheumatology. 2015; 11:462-474.
4. Almeida M, Han L, Martin-Millan M, Plotkin LI, Stewart SA, Roberson PK, Kousteni S, O'Brien CA, Bellido T, Parfitt AM, Weinstein RS, Jilka RL, Manolagas SC. Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. Journal of Biological Chemistry. 2007; 282: 27285-27297.
5. Almeida M, Han L, Ambrogini E, Bartell SM, Manolagas SC. Oxidative stress stimulates apoptosis and activates NFkappaB in osteoblastic cells via a PKCbeta/p66shc signaling cascade: counter regulation by estrogens or androgens. Molecular Endocrinolology. 2010; 24: 2030-2037.
6. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008; 132:27-42.
7. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature. 2008; 451:1069-1075.
8. Mizushima N. Autophagy: process and function. Genes & Development. 2007; 21: 2861-2873.
9. Kaur J, Debnath J. Autophagy at the crossroads of catabolism and anabolism. Nature Reviews Molecular Cellular Biology. 2015; 16: 461-472.
10. Pierrefite-Carle V, Santucci-Darmanin S, Breuil V, Camuzard O, Carle GF. Autophagy in bone: Self-eating to stay in balance. Ageing Research Reviews. 2015; 24:206-217.
11. Nollet M, Santucci-Darmanin S, Breuil V, Al-Sahlanee R, Cros C, Topi M, Momier D, Samson M, Pagnotta S, Cailleteau L, Battaglia S, Farlay D, Dacquin R et al. Autophagy in osteoblasts is involved in mineralization and bone homeostasis. Autophagy. 2014; 10:1965-1977.
12. Onal M, Piemontese M, Xiong J, Wang Y, Han L, Ye S, Komatsu M, Selig M, Weinstein RS, Zhao H, Jilka RL, Almeida M, Manolagas SC, et al. Suppression of autophagy in osteocytes mimics skeletal aging. Journal of Biological Chemistry. 2013; 288:17432-17440.
13. Liu F, Fang F, Yuan H, Yang D, Chen Y, Williams L, Goldstein SA, Krebsbach PH, Guan JL. Suppression of autophagy by FIP200 deletion leads to osteopenia in mice through the inhibition of osteoblast terminal differentiation. Journal of Bone and Mineral Research. 2013; 28:2414-2430.
14. DeSelm CJ, Miller BC, Zou W, Beatty WL, van Meel E, Takahata Y, Klumperman J, Tooze SA, Teitelbaum SL, Virgin HW. Autophagy proteins regulate the secretory component of osteoclastic bone resorption. Developmental Cell. 2011; 21: 966-974.
15. Zhang L, Guo YF, Liu YZ, Liu YJ, Xiong DH, Liu XG, Wang L, Yang TL, Lei SF, Guo Y, Yan H, Pei YF, Zhang F, et al. Pathway-based genome-wide association analysis identified the importance of regulation-of-autophagy pathway for ultradistal radius BMD. Journal of Bone and Mineral Research. 2010; 25:1572-1580.
16. Del Roso A, Vittorini S, Cavallini G, Donati A, Gori Z, Masini M, Pollera M, Bergamini E. Ageing-related changes in the in vivo function of rat liver macroautophagy and proteolysis. Experimental Gerontology. 2003; 38: 519-527.
17. Uddin MN, Nishio N, Ito S, Suzuki H, Isobe K. Autophagic activity in thymus and liver during aging. Age (Dordr). 2012; 34:75-85.
18. Rubinsztein DC, Marino G, Kroemer G. Autophagy and aging. Cell. 2011; 146: 682-695.
19. Russ DW, Boyd IM, McCoy KM, McCorkle KW. Musclespecificity of age-related changes in markers of autophagy and sphingolipid metabolism. Biogerontology. 2015; 16: 747-759.
20. Lipinski MM, Zheng B, Lu T, Yan Z, Py BF, Ng A, Xavier RJ, Li C, Yankner BA, Scherzer CR, Yuan J. Genomewide analysis reveals mechanisms modulating autophagy in normal brain aging and in Alzheimer's disease. Proceedings of the National Academy of Sciences U S A. 2010; 107: 14164-14169.
21. Chen K, Yang YH, Jiang SD, Jiang LS. Decreased activity of osteocyte autophagy with aging may contribute to the bone loss in senile population. Histochemistry Cell Biology. 2014; 142: 285-295.
22. Yang Y, Zheng X, Li B, Jiang S, Jiang L. Increased activity of osteocyte autophagy in ovariectomized rats and its correlation with oxidative stress status and bone loss. Biochemical and Biophysical Research Communications. 2014; 451: 86-92.
23. Bonewald LF. The amazing osteocyte. Journal of Bone and Mineral Research. 2011; 26: 229-238.
24. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, Adhihetty PJ, Adler SG, Agam G, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016; 12: 1-222.
25. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010; 140: 313-326.
26. Levasseur R, Barrios R, Elefteriou F, Glass DA, 2nd, Lieberman MW, Karsenty G. Reversible skeletal abnormalities in gamma-glutamyl transpeptidase-deficient mice. Endocrinology. 2003; 144: 2761-2764.
27. Lean JM, Davies JT, Fuller K, Jagger CJ, Kirstein B, Partington GA, Urry ZL, Chambers TJ. A crucial role for thiol antioxidants in estrogen-deficiency bone loss. Journal of Clinical Investigation. 2003; 112: 915-923.
28. Manolagas SC. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocrine Reviews. 2010; 31: 266-300.
29. Seo AY, Joseph A-M, Dutta D, Hwang JCY, Aris JP, Leeuwenburgh C. New insights into the role of mitochondria in aging: mitochondrial dynamics and more. J Cell Sci. 2010; 123: 2533-42
30. Lapierre LR, Kumsta C, Sandri M, Ballabio A, Hansen M. Transcriptional and epigenetic regulation of autophagy in aging. Autophagy. 2015; 11: 867-880.
31. Olivan S, Calvo AC, Manzano R, Zaragoza P, Osta R. Sex differences in constitutive autophagy. Biomed Research International. 2014; 2014: 652817.
32. Choi S, Shin H, Song H, Lim HJ. Suppression of autophagic activation in the mouse uterus by estrogen and progesterone. Journal of Endocrinology. 2014; 221: 39-50.
33. Wang F, Xiao J, Shen Y, Yao F, Chen Y. Estrogen protects cardiomyocytes against lipopolysaccharide by inhibiting autophagy. Molecular Medicine Reports. 2014; 10:1509-1512.
34. Lin CW, Chen B, Huang KL, Dai YS, Teng HL. Inhibition of Autophagy by Estradiol Promotes Locomotor Recovery after Spinal Cord Injury in Rats. Neuroscience Bulletin. 2016; 32: 137-144.
35. Yang YH, Chen K, Li B, Chen JW, Zheng XF, Wang YR, Jiang SD, Jiang LS. Estradiol inhibits osteoblast apoptosis via promotion of autophagy through the ER-ERK-mTOR pathway. Apoptosis. 2013; 18: 1363-1375.
36. White JP, Gao S, Puppa MJ, Sato S, Welle SL, Carson JA. Testosterone regulation of Akt/mTORC1/FoxO3a signaling in skeletal muscle. Molecular and Cellular Endocrinology. 2013; 365: 174-186.
37. Serra C, Sandor NL, Jang H, Lee D, Toraldo G, Guarneri T, Wong S, Zhang A, Guo W, Jasuja R, Bhasin S. The effects of testosterone deprivation and supplementation on proteasomal and autophagy activity in the skeletal muscle of the male mouse: differential effects on high-androgen responder and low-androgen responder muscle groups. Endocrinology. 2013; 154: 4594-4606.
38. Lahn BT, Page DC. Functional coherence of the human Y chromosome. Science. 1997; 278: 675-80.
39. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP, Frankish A, Lovell FL, Howe KL, et al. The DNA sequence of the human X chromosome. Nature. 2005; 434: 325-37.
40. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, Chinwalla A, Delehaunty A, Delehaunty K, et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature. 2003; 423: 825-37.
41. Malorni W, Straface E, Matarrese P, Ascione B, Coinu R, Canu S, Galluzzo P, Marino M, Franconi F. Redox state and gender differences in vascular smooth muscle cells. FEBS Lett. 2008; 582: 635-42.
42. Maselli A, Matarrese P, Straface E, Canu S, Franconi F, Malorni W. Cell sex: a new look at cell fate studies. FASEB J Off Publ Fed Am Soc Exp Biol. 2009; 23: 978-84.
43. Straface E, Vona R, Gambardella L, Ascione B, Marino M, Bulzomi P, Canu S, Coinu R, Rosano G, Malorni W, Franconi F. Cell sex determines anoikis resistance in vascular smooth muscle cells. FEBS Lett. 2009; 583: 3448-54.
44. Lista P, Straface E, Brunelleschi S, Franconi F, Malorni W. On the role of autophagy in human diseases: a gender perspective. Journal of Cellular and Molecular Medicine. 2011; 15: 1443-1457.
45. Turei D, Foldvari-Nagy L, Fazekas D, Modos D, Kubisch J, Kadlecsik T, Demeter A, Lenti K, Csermely P, Vellai T, Korcsmáros T. Autophagy Regulatory Network-a systemslevel bioinformatics resource for studying the mechanism and regulation of autophagy. Autophagy. 2015; 11: 155-165.
46. Prisby RD, Dominguez JM, 2nd, Muller-Delp J, Allen MR, Delp MD. Aging and estrogen status: a possible endothelium-dependent vascular coupling mechanism in bone remodeling. PLoS One. 2012; 7: e48564.
47. Blagosklonny MV. Validation of anti-aging drugs by treating age-related diseases. Aging. 2009; 1: 281-8. doi: 10.18632/aging.100034.
48. Bakker AD, Klein-Nulend J. Osteoblast isolation from murine calvaria and long bones. Methods in Molecular Biology. 2012; 816:19-29.
49. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature. 2006; 441: 885-9.
50. Dacquin R, Starbuck M, Schinke T, Karsenty G. Mouse alpha1(I)-collagen promoter is the best known promoter to drive efficient Cre recombinase expression in osteoblast. Developmental Dynamics. 2002; 224:245-251.