Protection against T1DM-induced bone loss by zinc supplementation: Biomechanical, histomorphometric, and molecular analyses in STZ-induced diabetic rats

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Bortolin, Raul Hernandes ^a   Abreu, Bento João Da Graça Azevedo ^a   Ururahy, Marcela Abbott Galvão ^a   De Souza, Karla Simone Costa ^a   Bezerra, João Felipe ^a   Loureiro, Melina Bezerra ^a   Da Silvada, Flávio Santos ^a   Marques, Dáfiny Emanuele Da Silva ^a   De Batista, Angélica Amanda Sousa ^c   Oliveira, Gisele ^c   Luchessi, André Ducati ^a   Lima, Valéria Morgiana Gualberto Duarte Moreira ^b   Miranda, Carlos Eduardo Saraiva ^c   Fook, Marcus Vinicius Lia ^d   Almeida, Maria Das Graç ^a   De Rezende, Luciana Augusto ^c   De Rezende, Adriana Augusto ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^b STATE UNIVERSITY OF PARAÍBA   (Brazil)

^c UNIVERSITY OF RIBEIRÃO PRETO   (Brazil)

^d FEDERAL UNIVERSITY OF CAMPINA GRANDE   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; COLLAGEN TYPE 1; GELATINASE B; MESSENGER RNA; OSTEOCALCIN; OSTEOPROTEGERIN; ZINC; COLLAGEN TYPE I, ALPHA 1 CHAIN; STREPTOZOCIN; TNFRSF11B PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BODY WEIGHT; BONE ATROPHY; BONE CHARACTERISTICS AND FUNCTIONS; BONE FLEXIBILITY; BONE STRENGTH; BONE STRUCTURE; COL1A GENE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; GENE; GENE EXPRESSION; HISTOPATHOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MMP 9 GENE; MORPHOMETRICS; NONHUMAN; OPG GENE; PROTEIN CONTENT; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ANIMAL; BONE DENSITY; CHEMICALLY INDUCED; DIET THERAPY; DIETARY SUPPLEMENT; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; FEMUR; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; OSTEOLYSIS; PATHOLOGY; PREVENTION AND CONTROL; TIBIA; WISTAR RAT; YOUNG MODULUS;

RATTUS; RATTUS NORVEGICUS;

ANIMALS; BIOMECHANICAL PHENOMENA; BONE DENSITY; BONE RESORPTION; COLLAGEN TYPE I; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIETARY SUPPLEMENTS; ELASTIC MODULUS; FEMUR; GENE EXPRESSION REGULATION; HUMANS; MALE; MATRIX METALLOPROTEINASE 9; OSTEOCALCIN; OSTEOPROTEGERIN; RATS; RATS, WISTAR; RNA, MESSENGER; STREPTOZOCIN; TIBIA; ZINC;

EID: 84928690029     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125349     Document Type: Article

References (76)

1. American Diabetes Association. Standards of medical care in diabetes - 2014. Diabetes Care. 2014; 37 Suppl 1: S14-S80. doi: 10.2337/dc14-S014 PMID: 24357209
2. Motyl K, McCabe LR. Streptozotocin, type I diabetes severity and bone. Biol Proced Online. 2009; 11: 296-315. doi: 10.1007/s12575-009-9000-5 PMID: 19495918
3. Thrailkill KM, Liu L, Wahl EC, Bunn RC, Perrien DS, Cockrell GE, et al. Bone formation is impaired in a model of type 1 diabetes. Diabetes. 2005; 54: 2875-2881. PMID: 16186388
4. Starup-Linde J. Diabetes, biochemical markers of bone turnover, diabetes control, and bone. Front Endocrinol (Lausanne). 2013; 4:21. doi: 10.3389/fendo.2013.00021 PMID: 23482417
5. Pietschmann P, Skalicky M, Kneissel M, Rauner M, Hofbauer G, Stupphann D, et al. Bone structure and metabolism in a rodent model of male senile osteoporosis. Exp Gerontol. 2007; 42: 1099-1108. PMID: 17949933
6. Hofbauer LC, Brueck CC, Singh SK, Dobnig H. Osteoporosis in patients with diabetes mellitus. J Bone Miner Res. 2007; 22: 1317-1328. PMID: 17501667
7. Prisby RD, Swift JM, Bloomfield SA, Hogan HA, Delp MD. Altered bone mass, geometry and mechanical properties during the development and progression of type 2 diabetes in the Zucker diabetic fatty rat. J Endocrinol. 2008; 199: 379-388. doi: 10.1677/JOE-08-0046 PMID: 18755885
8. Loureiro MB, Ururahy MA, Freire-Neto FP, Duarte VM, Oliveira GH, Hirata RDC, et al. Low bone mineral density is associated to poor glycemic control and increased OPG expression in children and adolescents with type 1 diabetes. Diabetes Res Clin Pract. 2014; 103: 452-457. doi: 10.1016/j.diabres.2013.12.018 PMID: 24529565
9. McCabe LR. Understanding the pathology and mechanisms of type I diabetic bone loss. J Cell Biochem. 2007; 102: 1343-1357. PMID: 17975793
10. Erdal N, Gürgül S, Demirel C, Yildiz A. The effect of insulin therapy on biomechanical deterioration of bone in streptozotocin (STZ)-induced type 1 diabetes mellitus in rats. Diabetes Res Clin Pract. 2012; 97: 461-467. doi: 10.1016/j.diabres.2012.03.005 PMID: 22483749
11. Reddy GK, Stehno-Bittel L, Hamade S, Enwemeka CS. The biomechanical integrity of bone in experimental diabetes. Diabetes Res Clin Pract. 2001; 54: 1-8. PMID: 11532324
12. Korres N, Tsiridis E, Pavlou G, Mitsoudis A, Perrea DN, Zoumbos AB, et al. Biomechanical characteristics of bone in streptozotocin-induced diabetic rats: An in-vivo randomized controlled experimental study. World J Orthop. 2013; 4: 124-129. doi: 10.5312/wjo.v4.i3.124 PMID: 23878780
13. Nyman JS, Lynch CC, Perrien DS, Thiolloy S, O'Quinn EC, Patil CA, et al. Differential effects between the loss of MMP-2 and MMP-9 on structural and tissue-level properties of bone. J Bone Miner Res. 2011; 26: 1252-1260. doi: 10.1002/jbmr.326 PMID: 21611966
14. Mohtai M, Smith RL, Schurman DJ, Tsuji Y, Torti FM, Hutchinson NI, et al. Expression of 92-kD type IV collagenase/gelatinase (gelatinase B) in osteoarthritic cartilage and its induction in normal human articular cartilage by interleukin 1. J Clin Invest. 1993; 92: 179-185. PMID: 8325982
15. Vandooren J, Van den Steen PE, Opdenakker G. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9): the next decade. Crit Rev Biochem Mol Biol. 2013; 48: 222-272. doi: 10.3109/10409238.2013.770819 PMID: 23547785
16. Zhang SQ, Chen GH, Lu WL, Zhang Q. Effects on the bones of vanadyl acetylacetonate by oral administration: a comparison study in diabetic rats. J Bone Miner Metab. 2007; 25: 293-301. PMID: 17704994
17. Cunha JS, Ferreira VM, Maquigussa E, Naves MA, Boim MA. Effects of high glucose and high insulin concentrations on osteoblast function in vitro. Cell Tissue Res. 2014; 358: 249-256. doi: 10.1007/s00441-014-1913-x PMID: 24859221
18. Wittrant Y, Gorin Y, Woodruff K, Horn D, Abboud HE, Mohan S, et al. High d(+)glucose concentration inhibits RANKL-induced osteoclastogenesis. Bone. 2008; 42: 1122-1130. doi: 10.1016/j.bone.2008.02.006 PMID: 18378205
19. Motyl KJ, Botolin S, Irwin R, Appledorn DM, Kadakia T, Amalfitano A, et al. Bone inflammation and altered gene expression with type I diabetes early onset. J Cell Physiol. 2009; 218: 575-583. doi: 10.1002/jcp.21626 PMID: 19006181
20. Amorim FP, Ornelas SS, Diniz SF, Batista AC, da Silva TA. Imbalance of RANK, RANKL and OPG expression during tibial fracture repair in diabetic rats. J Mol Histol. 2008; 39: 401-408. doi: 10.1007/s10735-008-9178-x PMID: 18592139
21. Yamaguchi M. Role of nutritional zinc in the prevention of osteoporosis. Mol Cell Biochem. 2010; 338: 241-254. doi: 10.1007/s11010-009-0358-0 PMID: 20035439
22. Yamaguchi M. Nutritional factors and bone homeostasis: synergistic effect with zinc and genistein in osteogenesis. Mol Cell Biochem. 2012; 366: 201-221. doi: 10.1007/s11010-012-1298-7 PMID: 22476903
23. Iitsuka N, Hie M, Tsukamoto I. Zinc supplementation inhibits the increase in osteoclastogenesis and decrease in osteoblastogenesis in streptozotocin-induced diabetic rats. Eur J Pharmacol. 2013; 714: 41-47. doi: 10.1016/j.ejphar.2013.05.020 PMID: 23735664
24. Ovesen J, Møller-Madsen B, Thomsen JS, Danscher G, Mosekilde L. The positive effects of zinc on skeletal strength in growing rats. Bone. 2001; 29: 565-570. PMID: 11728928
25. Brzóska MM, Galazyn-Sidorczuk M, Rogalska J, Roszczenko A, Jurczuk M, Majewska K, et al. Beneficial effect of zinc supplementation on biomechanical properties of femoral distal end and femoral diaphysis of male rats chronically exposed to cadmium. Chem Biol Interact. 2008; 171: 312-324. doi: 10.1016/j.cbi.2007.11.007 PMID: 18164699
26. Sunar F, Baltaci AK, Ergene N, Mogulkoc R. Zinc deficiency and supplementation in ovariectomized rats: their effect on serum estrogen and progesterone levels and their relation to calcium and phosphorus. Pak J Pharm Sci. 2009; 22: 150-154. PMID: 19339224
27. Abo-El-Asrar M, Farid SM, El Maraghy MO, Mohamedeen AK. Serum osteocalcin, zinc nutritive status and bone turnover in children and adolescents with type1 diabetes mellitus. J Diabetes Metab. 2011; 2: 128.
28. Yamaguchi M, Goto M, Uchiyama S, Nakagawa T. Effect of zinc on gene expression in osteoblastic MC3T3-E1 cells: enhancement of Runx2, OPG, and regucalcin mRNA expressions. Mol Cell Biochem. 2008; 312: 157-166. doi: 10.1007/s11010-008-9731-7 PMID: 18327666
29. Yamaguchi M, Uchiyama S. Preventive effect of zinc acexamate administration in streptozotocin-diabetic rats: restoration of bone loss. Int J Mol Med. 2003; 12: 755-761. PMID: 14533005
30. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the care and use of laboratory animals. 2011.
31. Melo MGD, Dória GAA, Serafini MR, Araújo AAS. Valores de referência Hematológicos e Bioquímicos de Ratos (Rattus novergicus linhagem Wistar) provenientes do biotério central da Universidade Federal de Sergipe. Scientia Plena. 2012; 8: 1-6.
32. Dantas JA, Ambiel CR, Cuman RKN, Baroni S, Bersani-Amado CA. Valores de referência de alguns parâmetros fisiológicos de ratos do Biotério Central da Universidade Estadual de Maringá, Estado do Paraná. Acta Sci Heal Sci. 2006; 28: 165-170.
33. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123: 1939-1951. PMID: 8229312
34. Duarte VM, Ramos AM, Rezende LA, Macedo UB, Brandão-Neto J, Almeida MG, et al. Osteopenia: a bone disorder associated with diabetes mellitus. J Bone Miner Metab. 2005; 23: 58-68. PMID: 15616896
35. Dempster DW, Compston JE, Drezner MK, Glorieux FH, Kanis JA, Malluche H, et al. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res. 2013; 28: 2-17. doi: 10.1002/jbmr.1805 PMID: 23197339
36. Rich L, Whittaker P. Collagen and picrosirius red staining: a polarized light assessment of fibrillar hue and spatial distribution. Brazilian J Morphol Sci. 2005; 22: 97-104.
37. Black MJ, D'Amore A, Auden A, Stamp L, Osicka T, Panagiotopoulos S, et al. Chronic type 1 diabetes in spontaneously hypertensive rats leads to exacerbated cardiac fibrosis. Cardiovasc Pathol. 2010; 19: 361-370. doi: 10.1016/j.carpath.2009.07.003 PMID: 19747849
38. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25: 402-408. PMID: 11846609
39. Goodman WG, Hori MT. Diminished bone formation in experimental diabetes. Relationship to osteoid maturation and mineralization. Diabetes. 1984; 33: 825-831. PMID: 6381178
40. Hamada Y, Kitazawa S, Kitazawa R, Fujii H, Kasuga M, Fukagawa M, et al. Histomorphometric analysis of diabetic osteopenia in streptozotocin-induced diabetic mice: a possible role of oxidative stress. Bone. 2007; 40: 1408-1414. PMID: 17251074
41. Hie M, Iitsuka N, Otsuka T, Tsukamoto I. Insulin-dependent diabetes mellitus decreases osteoblastogenesis associated with the inhibition of Wnt signaling through increased expression of Sost and Dkk1 and inhibition of Akt activation. Int J Mol Med. 2011; 28: 455-462. doi: 10.3892/ijmm.2011.697 PMID: 21567076
42. Uchiyama S, Yamaguchi M. Alteration in serum and bone component findings induced in streptozotocin-diabetic rats is restored by zinc acexamate. Int J Mol Med. 2003; 12: 949-954. PMID: 14612972
43. Bouillon R, Bex M, Van Herck E, Laureys J, Dooms L, Lesaffre E, et al. Influence of age, sex, and insulin on osteoblast function: osteoblast dysfunction in diabetes mellitus. J Clin Endocrinol Metab. 1995; 80: 1194-1202. PMID: 7714089
44. Kemink SA, Hermus AR, Swinkels LM, Lutterman JA, Smals AG. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest. 2000; 23: 295-303. PMID: 10882147
45. Auwerx J, Dequeker J, Bouillon R, Geusens P, Nijs J. Mineral metabolism and bone mass at peripheral and axial skeleton in diabetes mellitus. Diabetes. 1988; 37: 8-12. PMID: 3335279
46. Levin ME, Boisseau VC, Avioli LV. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med. 1976; 294: 241-245. PMID: 1244549
47. Tuominen JT, Impivaara O, Puukka P, Rönnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care. 1999; 22: 1196-1200. PMID: 10388989
48. Muñoz-Torres M, Jódar E, Escobar-Jiménez F, López-Ibarra PJ, Luna JD. Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif Tissue Int. 1996; 58: 316-319. PMID: 8661964
49. Buysschaert M, Cauwe F, Jamart J, Brichant C, De Coster P, Magnan A, et al. Proximal femur density in type 1 and 2 diabetic patients. Diabete Metab. 1992; 18: 32-37. PMID: 1563534
50. Botolin S, McCabe LR. Bone loss and increased bone adiposity in spontaneous and pharmacologically induced diabetic mice. Endocrinology. 2007; 148: 198-205. PMID: 17053023
51. Hadley KB, Newman SM, Hunt JR. Dietary zinc reduces osteoclast resorption activities and increases markers of osteoblast differentiation, matrix maturation, and mineralization in the long bones of growing rats. J Nutr Biochem. 2010; 21: 297-303. doi: 10.1016/j.jnutbio.2009.01.002 PMID: 19369052
52. Kwun IS, Cho YE, Lomeda RA, Shin HI, Choi JY, Kang YH, et al. Zinc deficiency suppresses matrix mineralization and retards osteogenesis transiently with catch-up possibly through Runx 2 modulation. Bone. 2010; 46: 732-741. doi: 10.1016/j.bone.2009.11.003 PMID: 19913120
53. Ryz NR, Weiler HA, Taylor CG. Zinc deficiency reduces bone mineral density in the spine of young adult rats: a pilot study. Ann Nutr Metab. 2009; 54: 218-226. doi: 10.1159/000224627 PMID: 19506366
54. Arreola F, Paniagua R, Díaz-Bensussen S, Urquieta B, López-Montaño E, Partida-Hernández G, et al. Bone mineral content, 25-hydroxycalciferol and zinc serum levels in insulin-dependent (type I) diabetic patients. Arch Invest Med (Mex). 1990; 21: 195-199. PMID: 2103709
55. Maser RE, Stabley JN, Lenhard MJ, Owusu-Griffin P, Provost-Craig MA, Farquhar WB, et al. Zinc intake and biochemical markers of bone turnover in type 1 diabetes. Diabetes Care. 2008; 31: 2279-2280. doi: 10.2337/dc08-1068 PMID: 18809628
56. Tsuchida T, Sato K, Miyakoshi N, Abe T, Kudo T, Tamura Y, et al. Histomorphometric evaluation of the recovering effect of human parathyroid hormone (1-34) on bone structure and turnover in streptozotocin-induced diabetic rats. Calcif Tissue Int. 2000; 66: 229-233. PMID: 10666500
57. Martin LM, McCabe LR. Type I diabetic bone phenotype is location but not gender dependent. Histochem Cell Biol. 2007; 128: 125-133. PMID: 17609971
58. Seino Y, Ishida H. Diabetic osteopenia: pathophysiology and clinical aspects. Diabetes Metab Rev. 1995; 11: 21-35. PMID: 7600905
59. Turner CH. Bone strength: current concepts. Ann N Y Acad Sci. 2006; 1068: 429-446. PMID: 16831941
60. Zhao H, Xia Z, Cai G, Du J, Zhu T, Shen L. Expression of type-I collagen and matrix metalloproteinase-9 mRNA in bone of castrated adult female rats: effects of estrogen. Chin Med J (Engl). 1998; 111: 551-555. PMID: 11245078
61. Okada Y, Naka K, Kawamura K, Matsumoto T, Nakanishi I, Fujimoto N, et al. Localization of matrix metalloproteinase 9 (92-kilodalton gelatinase/type IV collagenase = gelatinase B) in osteoclasts: implications for bone resorption. Lab Invest. 1995; 72: 311-322. PMID: 7898050
62. Grigoriadis AE, Wang ZQ, Cecchini MG, Hofstetter W, Felix R, Fleisch HA et al. c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science. 1994; 266: 443-448. PMID: 7939685
63. Lorenzo JA, Pilbeam CC, Kalinowski JF, Hibbs MS. Production of both 92- and 72-kDa gelatinases by bone cells. Matrix. 1992; 12: 282-290. PMID: 1435512
64. Uchiyama S, Yamaguchi M. Anabolic effect of beta-cryptoxanthin in osteoblastic MC3T3-E1 cells is enhanced with 17beta-estradiol, genistein, or zinc sulfate in vitro: the unique effect with zinc on Runx2 and alpha1(I) collagen mRNA expressions. Mol Cell Biochem. 2008; 307: 209-219. PMID: 17899321
65. Gur A, Colpan L, Cevik R, Nas K, Jale Sarac A. Comparison of zinc excretion and biochemical markers of bone remodelling in the assessment of the effects of alendronate and calcitonin on bone in postmenopausal osteoporosis. Clin Biochem. 2005; 38: 66-72. PMID: 15607319
66. Botolin S, McCabe LR. Chronic hyperglycemia modulates osteoblast gene expression through osmotic and non-osmotic pathways. J Cell Biochem. 2006; 99: 411-424. PMID: 16619259
67. Mizuno A, Amizuka N, Irie K, Murakami A, Fujise N, Kanno T, et al. Severe osteoporosis in mice lacking osteoclastogenesis inhibitory factor/osteoprotegerin. Biochem Biophys Res Commun. 1998; 247: 610-615. PMID: 9647741
68. Fong L, Tan K, Tran C, Cool J, Scherer MA, Elovaris R, et al. Interaction of dietary zinc and intracellular binding protein metallothionein in postnatal bone growth. Bone. 2009; 44: 1151-1162. doi: 10.1016/j.bone.2009.02.011 PMID: 19254786
69. Owen TA, Aronow M, Shalhoub V, Barone LM, Wilming L, Tassinari MS, et al. Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol. 1990; 143: 420-430. PMID: 1694181
70. Stein GS, Lian JB, Owen TA. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J. 1990; 4: 3111-3123. PMID: 2210157
71. Weinreb M, Shinar D, Rodan GA. Different pattern of alkaline phosphatase, osteopontin, and osteocalcin expression in developing rat bone visualized by in situ hybridization. J Bone Miner Res. 1990; 5: 831-842. PMID: 2239367
72. McCabe LR, Kockx M, Lian J, Stein J, Stein G. Selective expression of fos- and jun-related genes during osteoblast proliferation and differentiation. Exp Cell Res. 1995; 218: 255-262. PMID: 7737363
73. Ducy P, Desbois C, Boyce B, Pinero G, Story B, Dunstan C, et al. Increased bone formation in osteocalcin-deficient mice. Nature. 1996; 382: 448-452. PMID: 8684484
74. Fedde KN, Blair L, Silverstein J, Coburn SP, Ryan LM, Weinstein RS, et al. Alkaline phosphatase knock-out mice recapitulate the metabolic and skeletal defects of infantile hypophosphatasia. J Bone Miner Res. 1999; 14: 2015-2026. PMID: 10620060
75. Anderson HC, Sipe JB, Hessle L, Dhanyamraju R, Atti E, Camacho NP, et al. Impaired calcification around matrix vesicles of growth plate and bone in alkaline phosphatase-deficient mice. Am J Pathol. 2004; 164: 841-847. PMID: 14982838
76. Beattie JH, Avenell A. Trace element nutrition and bone metabolism. Nutr Res Rev. 1992; 5: 167-188. doi: 10.1079/NRR19920013 PMID: 19094319