Oral bovine lactoferrin improves bone status of ovariectomized mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 296, Issue 6, 2009, Pages

  Blais, Anne ^b,e   Malet, Arnaud ^a,b,c   Mikogami, Takashi ^c   Martin Rouas, Christine ^d   Tomé, Daniel ^a,b  

^a Inst de Rech de la Constr Navale   (France)

^b AGROPARISTECH   (France)

^c Armor Protéines ^*  (France)

^d Groupe Soparind Bongrain   (France)

^e INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Bone mineral density; Osteoblast; Osteoclast

Indexed keywords

LACTOFERRIN; MILK PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BONE DENSITY; BONE METABOLISM; CELL ACTIVITY; CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; CONTROLLED STUDY; DIET SUPPLEMENTATION; FEMALE; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOLYSIS; OVARIECTOMY; POSTMENOPAUSE; PRIORITY JOURNAL;

ADMINISTRATION, ORAL; ANIMAL FEED; ANIMALS; BIOMECHANICS; BODY COMPOSITION; BONE DENSITY; BONE RESORPTION; CATTLE; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; FEMUR; LACTOFERRIN; MICE; MICE, INBRED C3H; OSTEOBLASTS; OSTEOCLASTS; OVARIECTOMY; POSTMENOPAUSE;

EID: 66849091817     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.90938.2008     Document Type: Article

References (59)

1. Alexender JM, Bab I, Fish S, Mü ller R, Uchiyama T, Gronowicz G, Nahounou M, Zhao Q, White DW, Chorev M, Gazit D, Rosenblatt M. Human parathyroid hormone 1-34 reverses bone loss in ovariectomized mice. J Bone Miner Res 16: 1665-1673, 2001.
2. Aoe S, Toba Y, Yamamura J, Kawakami M, Yahiro M, Kumegawa M, Itabashi A, Takada Y. Controlled trial of the effects of milk basic protein (MBP) supplementation on bone metabolism in healty women. Biosci Biotechnol Biochem 65: 913-918, 2001. (Pubitemid 33614180)
3. Aoe S, Koyama T, Toba Y, Itabashi A, Takada Y. A controlled trial of the effect of milk basic protein (MBP) supplementation on bone metabolism in healthy menopausal women. Osteporos Int 16: 2123-2128, 2005. (Pubitemid 41790935)
4. Bouxsein ML, Myers KS, Shultz KL, Donahue LR, Rosen CJ, Beamer WG. Ovariectomy-induced bone loss varies among strains of mice. J Bone Miner Res 20: 1085-1092, 2005. (Pubitemid 40863796)
5. Cenci S, Weitzmann MN, Roggia C, Namba N, Novack D, Woodring J, Pacifici R. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest 106: 1229-1237, 2000.
6. Charatcharoenwitthaya N, Khosla S, Atkinson EJ, McCready LK, Riggs BL. Effect of blockade of TNF-alpha and interleukin-1 action on bone resorption in early postmenopausal women. J Bone Miner Res 22: 724-729, 2007.
7. Clowes JA, Riggs BL, Khosla S. The role of the immune system in the pathophysiology of osteoporosis. Immunol Rev 208: 207-227, 2005. (Pubitemid 41746395)
8. Cornish J, Callon KE, Naot D, Palmano KP, Banovic T, Bava U, Watson M, Lin JM, Tong PC, Chen Q, Chan VA, Reid HE, Fazzalari N, Baker HM, Baker EN, Haggarty NW, Grey AB, Reid IR. Lactoferrin is a potent regulator of bone cell activity and increases bone formation in vivo. Endocrinology 145: 4366-4374, 2004. (Pubitemid 39120586)
9. De Sousa M, Breedvelt F, Dynesius-Trentham R, Trentham D, Lum J. Iron, iron-binding proteins and immune system cells. Ann NY Acad Sci 526: 310-322, 1988. (Pubitemid 18201701)
10. Fischer R, Debbabi H, Blais A, Dubarry M, Rautureau M, Boyaka PN, Tome D. Uptake of ingested bovine lactoferrin and its accumulation in adult mouse tissues. Int Immunopharcol 7: 1387-1393, 2007. (Pubitemid 47161068)
11. Fujioka M, Uehara M, Wu J, Adlercreutz H, Suzuki K, Kanazawa K, Takeda K, Ishimi Y. Equol, a metabolite of diadzein, inhibits bone loss in ovaroectomized mice. J Nutr 143: 2623-2627, 2004. (Pubitemid 39315263)
12. Gahr M, Speer CP, Damereau B, Sawatzki G. Influence of lactoferrin on the function of human polymorphonuclear leukocytes and monocytes. J Leukoc Biol 49: 427-433, 1991.
13. Grassi F, Tell G, Robbie-Ryan M, Gao Y, Terauchi M, Yang X, Romanello M, Jones DP, Weitzmann MN, Pacifici R. Oxidative stress causes bone loss in estrogen-deficient mice through enhanced bone marrow dendritic cell activation. Proc Natl Acad Sci USA 104: 15087-15092, 2007. (Pubitemid 47619597)
14. Gentile P, Broxmeyer HE. Suppression of mouse myelopoiesis by administration of human lactoferrin in vivo and the comparative action of human transferrin. Blood 61: 982-993, 1983.
15. Harada E, Itoh Y, Sitizyo K, Takeuchi T, Araki Y, Kitagawa H. Characteristic transport of lactoferrin from the intestinal lumen into the bile via the blood in piglets. Comp Biochem Physiol A Mol Integr Physiol 124: 321-327, 1999.
16. Hayashida K, Kaneko T, Takeuchi T, Shimizu H, Ando K, Harada E. Oral administration of lactoferrin inhibits inflammation and nociception in rat adjuvant-induced arthritis. J Vet Med Sci 66: 149-154, 2004. (Pubitemid 41380329)
17. Hu WL, Mazurier J, Sawatzki G, Montreuil J, Spik G. Lactotransferrin receptor of mouse small-intestinal brush border. Binding characteristics of membrane-bound and triton X-100-solubilized forms. Biochem J 249: 435-441, 1988.
18. Hu WL, Mazurier J, Montreuil J, Spik G. Isolation and partial characterization of a lactotransferrin receptor from mouse intestinal brush border. Biochemistry 29: 535-541, 1990. (Pubitemid 20037662)
19. Ishimi Y, Miyaura C, Ohmura M, Onoe Y, Sato T, Uchiyama Y, Ito M, Wang X, Suda T, Ikegami S. Selective effects of genistein, a soybean isoflavone, on B-lymphopoiesis and bone loss caused by estrogen deficiency. Endocrinology 140: 1893-1900, 1999. (Pubitemid 29149263)
20. Jepsen KJ, Akkus OJ, Majeska RJ, Nadeau JH. Hierarchical relationship between bone traits and mechanical properties in inbred mice. Mamm Genome 14: 97-104, 2003. (Pubitemid 36241337)
21. Kimble RB, Bain S, Pacifici R. The functional block of TNF but not of IL-6 prevents bone loss in ovariectomized mice. J Bone Miner Res 12: 935-941, 1997. (Pubitemid 27225004)
22. Kuwata H, Yip TT, Yamauchi K, Teraguchi S, Hayasawa H, Tomita M, Hutchens TW. The survival of ingested lactoferrin in the gastrointestinal tract of adult mice. Biochem J 334: 321-323, 1998. (Pubitemid 28448574)
23. 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. J Clin Invest 112: 915-923, 2003. (Pubitemid 38063749)
24. Le Magnen C, Rainard P, Maubois JL, Paraf A, Phan Thanh L. Enzyme linked immunosorbent assay for bovine lactoferrin titration. Le Lait 69: 23-28, 1989.
25. Legrand D, Elass E, Pierce A, Mazurier J. Lactoferrin and host defence: an overview of its immuno-modulating and anti-inflammatory properties. Biometals 17: 225-229, 2004. (Pubitemid 38987141)
26. Legrand D, Elass E, Carpentier M, Mazurier J. Interaction of lactoferrin with cells involved in immune function. Biochem Cell Biol 84: 282-290, 2005.
27. Levay PF, Viljeon M. Lactoferrin: a general review. Heamatologica 80: 252-267, 1995.
28. Li CY, Schaffler MB, Wolde-Semait HT, Hernandez CJ, Jepsen KJ. Genetic background influences cortical bone response to ovariectomy. J Bone Miner Res 20: 2150-2158, 2005. (Pubitemid 41698778)
29. Lönnerdal B, Iyer S. Lactoferrin: molecular stucture and biological function. Ann Rev Nutr 15: 93-110, 1995.
30. Lorenzo JA, Naprta A, Rao Y, Alander C, Glaccum M, Widmer M, Gronowicz G, Kalinowski J, Pilbeam CC. Mice lacking the type I interleukin-1 receptor do not lose bone mass after ovariectomy. Endocrinology 139: 3022-3025, 1998. (Pubitemid 28512417)
31. Lorget F, Clough J, Oliveira M, Daury MC, Sabokbar A, Offord E. Lactoferrin reduces in vitro osteoclast differentiation and resorbing activity. Biochem Biophys Res Commun 296: 261-266, 2002.
32. Matsuoka Y, Serizawa A, Yoshioka T, Yamamura J, Morita Y, Kawakami H, Toba Y, Takada Y, Kumegawa M. Cystatin C in milk basic protein (MBP) and its inhibitory effect on bone resorption in vitro. Biosci Biotechnol Biochem 66: 2531-2536, 2002. (Pubitemid 39251121)
33. Morita Y, Matsuyama H, Serizawa A, Takeya T, Kawakami H. Identification of angiogenin as the osteoclastic bone resorption-inhibitory factor in bovine milk. Bone 42: 380-387, 2008.
34. Muthusami S, Ramachandran I, Muthusamy B, Vasudevan G, Prabhu V, Subramaniam V, Jagadeesan A, Narasimhan S. Ovariectomy induces oxidative stress and impairs bone antioxidant system in adult rats. Clin Chim Acta 360: 81-86, 2005. (Pubitemid 41225396)
35. Oh SM, Lee SH, Lee BJ, Pyo CW, Yoo NK, Lee SY, Kim J, Choi SY. A distinct role of neutrophil lactoferrin in RelA/p65 phosphorylation on Ser536 by recruiting TNF receptor-associated factors to IkappaB kinase signaling complex. J Immunol 179: 5686-5692, 2007.
36. Ohnishi H, Nakamura T, Narusawa K, Narakami H, Abe M, Barbier A, Suzuki K. Bisphosphonate tiludronate increases bone strength by improving mass and structure in established osteopenia after ovariectomy in rats. Bone 21: 335-343, 1997. (Pubitemid 27454087)
37. Omi N, Ezawa I. The effect of ovariectomy on bone metabolism in rats. Bone 17: 163S-168S, 1995.
38. Pacifici R, Brown C, Puscheck E, Friedrich E, Slatopolsky E, Maggio D, McCracken R, Avioli LV. Effect of surgical menopause and estrogen replacement on cytokine release from human blood mononuclear cells. Proc Natl Acad Sci USA 88: 5134-5138, 1991. (Pubitemid 21914698)
39. Pfeilschifter J, Koditz R, Pfohl M, Schatz H. Changes in proinflammatory cytokine after menopause. Endocr Rev 23: 90-119, 2002. (Pubitemid 34185307)
40. Roggia C, Gao Y, Cenci S, Weitzmann MN, Toraldo G, Isaia G, Pacifici R. Up-regulation of TNF-producing T cells in the bone marrow: a key mechanism by which estrogen deficiency induces bone loss in vivo. Proc Natl Acad Sci USA 98: 13960-13965, 2001. (Pubitemid 33116006)
41. Sakai A, Nishida S, Okimoto N, Okazaki Y, Hirano T, Norimura T, Suda T. Bone marrow cell development and trabecular bone dynamics after ovariectomy in ddy mice. Bone 23: 443-451, 1998. (Pubitemid 28470614)
42. Sawatzki G, Rich IN. Lactoferrin stimulates colony stimulating factor production in vitro and in vivo. Blood Cells 15: 371-385, 1989. (Pubitemid 19147925)
43. Seibel MJ. Biochemical markers of bone turnover: part I: biochemistry and variability. Clin Biocem Rev 26: 97-122, 2005.
44. Shanker G, Sorci-Thomas M, Adams MR. Estrogen modulates the expression of tumor necrosis factor alpha mRNA in phorbol ester-stimulated human monocytic THP-1 cells. Lymphokine Cytokine Res 13: 377-382, 1994.
45. Silverman N, Maniatis T. NF-kappaB signaling pathways in mammalian and insect innate immunity. Genes Dev 15: 2321-2342, 2001. (Pubitemid 32899738)
46. Spagnuolo PA, Bird RP, Hoffman-Goetz L. Effect of short-term dietary intake of bovine lactoferrin on intestinal lymphocyte apoptosis in healthy mice. Nutrition 23: 812-817, 2007. (Pubitemid 47532390)
47. Suda T, Takahashi N, Udagawa N, Jimi E, Gillespie MT, Martin TJ. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 20: 345-357, 1999. (Pubitemid 30649812)
48. Uenishi K, Ishida H, Toba Y, Aoe S, Itabashi A, Takada Y. Milk basic protein increases bone mineral density and improves bone metabolism in healthy young women. Osteporos Int 18: 385-390, 2007. (Pubitemid 46233185)
49. Van Veen HA, Geerts ME, van Berkel PH, Nuijens JH. The role of N-linked glycosylation in the protection of human and bovine lactoferrin against tryptic proteolysis. Eur J Biochem 271: 678-684, 2004. (Pubitemid 38250910)
50. Ward WE, Fonseca D. Soy isoflavones and fatty acids: effects on bone tissue postovariectomy in mice. Mol Nutr Food Res 51: 824-831, 2007. (Pubitemid 47173692)
51. Weitzmann MN, Pacifici R. Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 116: 1186-1194, 2006.
52. Weitzmann MN, Pacifici R. T cells: unexpected players in the bone loss induced by estrogen deficiency and in basal bone homeostasis. Ann NY Acad Sci 1116: 360-375, 2007. (Pubitemid 350274346)
53. Wronski TJ, Dann LM, Scott KS, Cintron M. Long-term effects of ovariectomy and aging on the rat skeleton. Calcif Tissue Int 45: 360-366, 1989. (Pubitemid 20028364)
54. Wu J, Wang XX, Takasaki M, Ohta A, Higuchi M, Ishimi Y. Cooperative effects of exercise training and genistein administration on bone mass in ovariectomized mice. J Bone Miner Res 16: 1829-1836, 2001. (Pubitemid 32911489)
55. Yamamura J, Takada Y, Goto M, Kumegawa M, Aoe S. High mobility group-like protein in bovine milk stimulates the proliferation of osteoblastic MC3T3-E1 cells. Biochem Biophys Res Commun 261: 113-117, 1999. (Pubitemid 29371627)
56. Yamamura J, Takada Y, Goto M, Kumegawa M, Aoe S. Bovine milk kininogen fragment 1.2 promotes the proliferation of osteoblastic MC3T3-E1 cells. Biochem Biophys Res Commun 269: 628-632, 2000. (Pubitemid 30440352)
57. Yamamura J, Aoe S, Toba Y, Motouri M, Kawakami H, Kumegawa M, Itabashi A, Takada Y. Milk basic protein (MBP) increases radial bone mineral density in healthy adult women. Biosci Biotechnol Biochem 66: 702-704, 2002. (Pubitemid 39251039)
58. Yamamura J, Morita Y, Takada Y, Kawakami H. The fragments of bovine high molecular weight kininogen promote osteoblast proliferation in vitro. J Biochem 140: 825-830, 2006. (Pubitemid 46941012)
59. Zhou H, Iida-Klein A, Lu SS, Ducayen-Knowles M, Levine LR, Dempster DW, Lindsay R. Anabolic action of parathyroid hormone on cortical and cancellous bone differs between axial and appendicular skeletal sites in mice. Bone 32: 513-520, 2003. (Pubitemid 39665710)