Low levels of plasma IGF-1 inhibit intracortical bone remodeling during aging

Age

Volumn 35, Issue 5, 2013, Pages 1691-1703

  Courtland, Hayden William ^a   Kennedy, Oran D ^b   Wu, Yingjie ^a,c   Gao, Ying ^a   Sun, Hui ^a,c   Schaffler, Mitchell B ^b   Yakar, Shoshana ^a,c  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c NEW YORK UNIVERSITY COLLEGE OF DENTISTRY   (United States)

Author keywords

Aging; ALSKO mice; Bone; Endocrine; IGF 1; Microcomputed tomography

Indexed keywords

SOMATOMEDIN C;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE REMODELING; BONE STRENGTH; BONE TISSUE; CONTROLLED STUDY; CORTICAL BONE; FAT MASS; GENE DELETION; LEAN BODY WEIGHT; MALE; MOUSE; NONHUMAN; OSTEOLYSIS; PHENOTYPE; POROSITY; PROTEIN BLOOD LEVEL; RIGIDITY;

AGING; ANIMALS; BONE DENSITY; BONE REMODELING; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMUR; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOCLASTS; OSTEOPOROSIS;

EID: 84892587966     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-012-9469-8     Document Type: Article

References (44)

1. 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 (2007) Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282 (37):27285-27297
2. Bagi CM, Ammann P, Rizzoli R, Miller SC (1997) Effect of estrogen deficiency on cancellous and cortical bone structure and strength of the femoral neck in rats. Calcif Tissue Int 61 (4):336-344
3. Bartke A, Brown-Borg H (2004) Life extension in the dwarf mouse. Curr Top Dev Biol 63:189-225
4. Boonen S, Mohan S, Dequeker J, Aerssens J, Vanderschueren D, Verbeke G, Broos P, Bouillon R, Baylink DJ (1999) Down-regulation of the serum stimulatory components of the insulin-like growth factor (IGF) system (IGF-I, IGF-II, IGF binding protein [BP]-3, and IGFBP-5) in age-related (type II) femoral neck osteoporosis. J Bone Miner Res 14 (12):2150-2158
5. Boyce TM, Bloebaum RD (1993) Cortical aging differences and fracture implications for the human femoral neck. Bone 14 (5):769-778
6. Cardoso L, Herman BC, Verborgt O, Laudier D, Majeska RJ, Schaffler MB (2009) Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue. J Bone Miner Res 24(4):597-605
7. Chavassieux P, Garnero P, Duboeuf F, Vergnaud P, Brunner- Ferber F, Delmas PD, Meunier PJ (2001) Effects of a new selective estrogen receptor modulator (MDL 103,323) on cancellous and cortical bone in ovariectomized ewes: a biochemical, histomorphometric, and densitometric study. J Bone Miner Res 16(1):89-96
8. Courtland HW, DeMambro V, Maynard J, Sun H, Elis S, Rosen C, Yakar S (2010) Sex-specific regulation of body size and bone slenderness by the acid labile subunit. J Bone Miner Res 25(9):2059-2068
9. Courtland HW, Elis S, Wu Y, Sun H, Rosen CJ, Jepsen KJ, Yakar S (2011) Serum IGF-1 affects skeletal acquisition in a temporal and compartment-specific manner. PLoS One 6 (3):e14762
10. Djuric M, Djonic D, Milovanovic P, Nikolic S, Marshall R, Marinkovic J, Hahn M (2010) Region-specific sexdependent pattern of age-related changes of proximal femoral cancellous bone and its implications on differential bone fragility. Calcif Tissue Int 86(3):192-201
11. Elis S, Courtland HW, Wu Y, Rosen CJ, Sun H, Jepsen KJ, Majeska RJ, Yakar S (2010) Elevated serum levels of IGF-1 are sufficient to establish normal body size and skeletal properties even in the absence of tissue IGF-1. J BoneMiner Res 25(6):1257-1266
12. Fritton JC, Kawashima Y, Mejia W, Courtland HW, Elis S, Sun H, Wu Y, Rosen CJ, Clemmons D, Yakar S (2010) The insulin-like growth factor-1 binding protein acid-labile subunit alters mesenchymal stromal cell fate. J Biol Chem 285(7):4709-4714
13. Gillberg P, Olofsson H, Mallmin H, Blum WF, Ljunghall S, Nilsson AG (2002) Bone mineral density in femoral neck is positively correlated to circulating insulin-like growth factor (IGF)-I and IGF-binding protein (IGFBP)-3 in Swedish men. Calcif Tissue Int 70(1):22-29
14. Halloran BP, Ferguson VL, Simske SJ, Burghardt A, Venton LL, Majumdar S (2002) Changes in bone structure and mass with advancing age in the male C57BL/6J mouse. J Bone Miner Res 17(6):1044-1050
15. Hauck SJ, Bartke A (2000) Effects of growth hormone on hypothalamic catalase and Cu/Zn superoxide dismutase. Free Radic Biol Med 28(6):970-978
16. Kennedy OD, Herman BC, Laudier DM, Majeska RJ, Sun HB, Schaffler MB (2012) Activation of resorption in fatigue-loaded bone involves both apoptosis and active pro-osteoclastogenic signaling by distinct osteocyte populations. Bone 50 (5):1115-1122
17. Langlois JA, Rosen CJ, Visser M, Hannan MT, Harris T, Wilson PW, Kiel DP (1998) Association between insulin-like growth factor I and bone mineral density in older women and men: the Framingham Heart Study. J Clin Endocrinol Metab 83(12):4257-4262
18. Lauritzen DB, Balena R, Shea M, Seedor JG, Markatos A, Le HM, Toolan BC, Myers ER, Rodan GA, Hayes WC (1993) Effects of combined prostaglandin and alendronate treatment on the histomorphometry and biomechanical properties of bone in ovariectomized rats. J Bone Miner Res 8(7):871-879
19. Lochmuller EM, Matsuura M, Bauer J, Hitzl W, Link TM, Muller R, Eckstein F (2008) Site-specific deterioration of trabecular bone architecture in men and women with advancing age. J Bone Miner Res 23(12):1964-1973
20. Mann V, Huber C, Kogianni G, Collins F, Noble B (2007) The antioxidant effect of estrogen and selective estrogen receptor modulators in the inhibition of osteocyte apoptosis in vitro. Bone 40(3):674-684
21. McCalden RW, McGeough JA, Barker MB, Court-Brown CM (1993) Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg Am 75 (8):1193-1205
22. Melton LJ 3rd, Rigss BL, Keaveny TM, Achenbach SJ, Hoffmann PF, Camp JJ, Rouleau PA, Bouxsein ML, Amin S, Atkinson EJ, Robb RA, Khosla S (2007) Structural determinants of vertebral fracture risk. J Bone Miner Res 22(12):1885-1892
23. Mezquita-Raya P, Munoz-Torres M, Alonso G, de Luna JD, Quesada JM, Dorado G, Luque-Recio F, Ruiz-Requena ME, Lopez-Rodriguez F, Escobar-Jimenez F (2004) Susceptibility for postmenopausal osteoporosis: interaction between genetic, hormonal and lifestyle factors. Calcif Tissue Int 75(5):373-379
24. Patel MB, Arden NK, Masterson LM, Phillips DI, Swaminathan R, Syddall HE, Byrne CD, Wood PJ, Cooper C, Holt RI (2005) Investigating the role of the growth hormoneinsulin- like growth factor (GH-IGF) axis as a determinant of male bone mineral density (BMD). Bone 37(6):833-841
25. Perkins SL, Gibbons R, Kling S, Kahn AJ (1994) Age-related bone loss in mice is associated with an increased osteoclast progenitor pool. Bone 15(1):65-72
26. Price C, Herman BC, Lufkin T, Goldman HM, Jepsen KJ (2005) Genetic variation in bone growth patterns defines adult mouse bone fragility. J Bone Miner Res 20(11):1983-1991
27. Rhee EJ, Oh KW, Lee WY, Kim SW, Oh ES, Baek KH, Kang MI, Park CY, Choi MG, Yoo HJ, Park SW (2004) Age, body mass index, current smoking history, and serum insulin-like growth factor-I levels associated with bone mineral density in middle-aged Korean men. J Bone Miner Metab 22(4):392-398
28. Rivadeneira F, ZillikensMC, De Laet CE, Hofman A, Uitterlinden AG, Beck TJ, PolsHA(2007) Femoral neck BMD is a strong predictor of hip fracture susceptibility in elderly men and women because it detects cortical bone instability: the Rotterdam Study. J Bone Miner Res 22(11):1781-1790
29. Ruff CB, Hayes WC (1984) Age changes in geometry and mineral content of the lower limb bones. Ann Biomed Eng 12(6):573-584
30. Salmon AB, Murakami S, Bartke A, Kopchick J, Yasumura K, Miller RA (2005) Fibroblast cell lines from young adult mice of long-lived mutant strains are resistant to multiple forms of stress. Am J Physiol Endocrinol Metab 289(1): E23-E29
31. Sietsema WK (1995) Animal models of cortical porosity. Bone 17(4 Suppl):297S-305S
32. Silbermann M, Weiss A, Reznick AZ, Eilam Y, Szydel N, Gershon D (1987) Age-related trend for osteopenia in femurs of female C57BL/6 mice. Compr Gerontol [A] 1 (1):45-51
33. Simmons ED Jr, Pritzker KP, Grynpas MD (1991) Age-related changes in the human femoral cortex. J Orthop Res 9 (2):155-167
34. Sornay-Rendu E, Cabrera-Bravo JL, Boutroy S, Munoz F, Delmas PD (2009) Severity of vertebral fractures is associated with alterations of cortical architecture in postmenopausal women. J Bone Miner Res 24(4):737-743
35. Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas PD (2006) Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res 21(12):1856-1863
36. Verborgt O, Tatton NA, Majeska RJ, Schaffler MB (2002) Spatial distribution of Bax and Bcl-2 in osteocytes after bone fatigue: complementary roles in bone remodeling regulation? J Bone Miner Res 17(5):907-914
37. Weiss A, Arbell I, Steinhagen-Thiessen E, Silbermann M (1991) Structural changes in aging bone: osteopenia in the proximal femurs of female mice. Bone 12(3):165-172
38. Wergedal JE, Sheng MH, Ackert-Bicknell CL, Beamer WG, Baylink DJ (2005) Genetic variation in femur extrinsic strength in 29 different inbred strains of mice is dependent on variations in femur cross-sectional geometry and bone density. Bone 36(1):111-122
39. Wilson AK, Bhattacharyya MH, Miller S, Mani A, Sacco-Gibson N (1998) Ovariectomy-induced changes in aged beagles: histomorphometry of rib cortical bone. Calcif Tissue Int 62 (3):237-243
40. Yakar S, Liu JL, Stannard B, Butler A, Accili D, Sauer B, LeRoith D (1999) Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc Natl Acad Sci U S A 96(13):7324-7329
41. Yakar S, Rosen CJ, Beamer WG, Ackert-Bicknell CL, Wu Y, Liu JL, Ooi GT, Setser J, Frystyk J, Boisclair YR, LeRoith D (2002) Circulating levels of IGF-1 directly regulate bone growth and density. J Clin Invest 110(6):771-781
42. Yakar S, Bouxsein ML, Canalis E, Sun H, Glatt V, Gundberg C, Cohen P, Hwang D, Boisclair Y, Leroith D, Rosen CJ (2006) The ternary IGF complex influences postnatal bone acquisition and the skeletal response to intermittent parathyroid hormone. J Endocrinol 189(2):289-299
43. Yakar S, Canalis E, Sun H, Mejia W, Kawashima Y, Nasser P, Courtland HW, Williams V, Bouxsein M, Rosen C, Jepsen KJ (2009a) Serum IGF-1 determines skeletal strength by regulating subperiosteal expansion and trait interactions. J Bone Miner Res 24(8):1481-1492
44. Yakar S, Rosen CJ, Bouxsein ML, Sun H, Mejia W, Kawashima Y, Wu Y, Emerton K, Williams V, Jepsen K, Schaffler MB, Majeska RJ, Gavrilova O, Gutierrez M, Hwang D, Pennisi P, Frystyk J, Boisclair Y, Pintar J, Jasper H, Domene H, Cohen P, Clemmons D, LeRoith D (2009b) Serum complexes of insulin-like growth factor-1 modulate skeletal integrity and carbohydrate metabolism. FASEB J 23(3):709-719