Systematic analysis of molecular and physiological synergic effects of iron, manganese and copper on connective tissue

Н. В. Керимкулова, И. Ю. Торшин, О. А. Громова, В. Н. Серов, Н. В. Никифорова

Abstract


The present article provides systematic analysis of exposure of iron and its synergists copper and manganese on structure of connective tissue. The bio-information analysis of molecular mechanisms was made which are responsiblefor support of the physiological processes. In general, data from molecular-biological, experimental and clinical studies shows signifi cance of use of organic iron, copper and manganese preparations in prophylaxis and therapy of connective tissue disorders.


Keywords


pregnancy; connective tissue dysplasia; anemia; ferrous gluconate; copper; manganese; Tothema®

References


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Mikhailova AV, Smolenskii AV Clinicalfeatures and physicalfi tness parameters in athletes with cardiac connective tissue dysplasia syndrome. Klin Med (Mosk.) 2004; 82 (8): 44-8.

Zakhar’ian AL, Zakhar’ian EA The severity of varicose vein disease of the lower extremities in various degree of the connective tissue dysplasia syndrome. KlinKhir 2005; 8:42 -4.

Torshin IY, Gromova OA Molecular mechanisms of magnesium and connective tissue dysplasia. Rus. Med. Journal. 2008: 263-9.

Domnitskaia TM, D’iachenko AV, Kupriianova OO, Domnitskii MMV Clinical value of the use of magnesium orotate in adolescents with syndrome of cardiac connective tissue dysplasia. Kardiologiia 2005; 45 (3): 76-81.

Torshin IYu Bioinformatics in the post-genomic era: sensing the change from molecular genetics to personalized medicine. Nova Biomedical Books, NY, USA, 2009. In «Bioinformatics in the Post-GenomicEra» series.

Alberts B, Johnson A, LewisJ et al. Molecular Biology of the Cell, 4th edition, Garland Science, 2002.

Diaz-Castro J, Lopez-Frias MR, Campos MS et al. Severe nutritional iron-defi ciency anaemia has a negative eff ect on some bone turnover biomar-kers in rats. Eur JNutr 2011.

Fadda M, Zirattu G, Espa E, Orani GMorphological aspects of the synovial membrane and femoral epiphyseal cartilage in experimentally induced chronic anemia. Ital J Orthop Traumatol 1992; 18 (2): 271-7.

Jorgensen L, Skjelbakken T, Lochen ML et al. Anemia and the risk ofnon-vertebral fractures: the Tromso Study. Osteoporos Int 2010; 21 (10):1761-8

Chen Z, Thomson CA, Aickin M et al. The relationship between incidence of fractures and anemia in older multiethnic women. J Am Geriatr Soc 2010;58 (12): 2337-44 doi.

Abraham R, WaltonJ, Russell L et al. Dietary determinants of postmenopausal bone loss at the lumbar spine: a possible benefi cial eff ect of iron. Osteoporos Int 2006; 17 (8): 1165-73.

Goerss JB, Kim CH, Atkinson EJ et al. Risk of fractures in patients with pernicious anemia. J Bone Miner Res 1992; 7 (5): 573-9.

Smoliar VI Eff ect of iron-defi cient diets on the formation of bone tissue. VoprPitan 1984; (5): 55-915. Mamedov LA, Kosaganova NIu, Rikhireva GT et al. Changes in the content of transferrin, ceruloplasmin, iron, and copper in blood serum and granulation tissue in wound healing in an experiment. Patol Fiziol Eksp Ter 1988; 4:58-61.

O’Dell BL Roles for iron and copper in connective tissue biosynthesis. Philos TransR SocLondBBiolSci 1981; 294 (1071):91-104.

Yeowell HN, Walker LC Ehlers-Danlos syndrome type VI results from a nonsense mutation and a splice sitemediated exon-skipping mutation in the lysyl hydroxylase gene. ProcAssocAm Physicians 1997; 109 (4): 383-96.

Van der Slot AJ, Zuurmond AM et al. Identifi cation of PLOD2 as telopep-tide lysyl hydroxylase, an important enzyme in fi brosis. J Biol Chem 2003; 278 (42):40967-72.

Ha VT, Marshall MK, Elsas LJ et al. A patient with Ehlers-Danlos syndrome type VI is a compound heterozygote for mutations in the lysyl hydro-xylase gene. J Clin Invest 1994; 93 (4): 1716-21.

Cabral WA, Chang W, Barnes AM et al. Prolyl 3-hydroxylase 1 defi ciency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat Genet 2007; 39 (3): 359-65.

Yamasaki K, Hagiwara H Excess iron inhibits osteoblast metabolism. Toxicol Lett 2009; 191 (2-3): 211-5. Epub 2009

Giordano N, Vaccai D, Cintorino M et al. Histopathological study of iron deposit distribution in the rheumatoid synovium. Clin Exp Rheumatol 1991;9 (5):463-7.

Sindrilaru A, Peters T, Wieschalka S et al. An unrestrained proinfl amma-tory M1 macrophage population induced by iron impairs wound healing in humans and mice. J Clin Invest 2011; 121 (3): 985-97 doi.

Jacob AK, Hotchkiss RS, DeMeester SL et al. Endothelial cell apoptosis is accelerated by inorganic iron and heat via an oxygen radical dependent mechanism. Surgery 1997; 122 (2): 243-53.

Torshin IY, Gromova OA Hadzhidis AK Systematic analysis of the molecular mechanisms of iron, copper and manganese action in the pathogenesis of iron defi ciency anemia. Clinical pharmacology. 2010 3.

Branda SS, Yang ZY, Chew A, Isaya G Mitochondrial intermediate peptidase and the yeast frataxin homolog together maintain mitochondrial iron homeostasis in Saccharomyces cerevisiae. Hum Mol Genet 1999; 8 (6): 1099-110.

Reeves PG, DeMars LC Copper defi ciency reduces iron absorption and biological half-life in male rats. J Nutr2004;

(8): 1953-7.

Broker S, Meunier B, Rich P et al.MtDNA mutations associated with si-deroblastic anaemia cause a defect of mitochondrial cytochrome c oxi-dase. Eur J Biochem 1998; 258 (1): 132-8.

Bannister JV, Bannister WH, Rotilio G Aspects of the structure, function, and applications of superoxide dismutase. CRC Crit Rev Biochem 1987; 22 (2): 111-80.

Zhang CM, Chi X, Wang B et al. Downregulation of STEAP4, a highly-expressed TNF-alpha-inducible gene in adipose tissue, is associated with obesity in humans. Acta Pharmacol Sin 2008; 29 (5):587-92.

Borkow G, Gabbay J, Dardik R et al. Molecular mechanisms of enhanced wound healing by copper oxide-impregnated dressings. Wound Repair Regen 2010; 18 (2): 266-7532. Cangul IT, Gul NY, Topal A, Yilmaz R. Evaluation of the eff ects of topical tripeptide-copper complex and zinc oxide on open wound healing in rabbits. Vet Dermatol 2006; 17 (6): 417-23.

Sen CK, Khanna S, Venojarvi M et al. Copper-induced vascular endothelial growth factor expression and wound healing. Am J Physiol Heart Circ Physiol 2002; 282 (5): H1821-H1827.

Dickson KA, Kang DK, Kwon YS et al. Ribonuclease inhibitor regulates neovascularization by human angiogenin. Biochemistry 2009; 48 (18):3804-6.

La Mendola D, Magri A, Vagliasindi LI et al. Copper (II) complexformation with a linear peptide encompassing the putative cell binding site of angiogenin. Dalton Trans 2010; 39 (44): 10678-84.

Soncin F, Guitton JD, Cartwright T, Badet JInteraction of human angio-genin with copper modulates angiogenin binding to endothelial cells. Bio-chem BiophysRes Commun 1997; 236 (3): 604-10.

Lowe NM, Lowe NM, Fraser WD, Jackson MJ Is there a potential therapeutic value of copper and zinc for osteoporosis? Proc Nutr Soc 2002; 61 (2): 181-5.

Smoliar VI, Biniashevskii EV [Eff ect of copper defi ciency on growth and bone tissue formation]. Vopr Pitan 1988; (6): 28-32.

Jonas J, Burns J, Abel EW et al. Impaired mechanical strength of bone in experimental copper defi ciency. Ann Nutr Metab 1993; 37 (5): 245-52.

Opsahl W, Zeronian H, Ellison M et al. Role of copper in collagen cross-linking and its infl uence on selected mechanical properties of chick bone and tendon. JNutr 1982; 112 (4): 708-16.

Borg TK, Klevay LM, Gay RE et al. Alteration of the connective tissue network of striated muscle in copper defi cient rats. J Mol Cell Cardiol 1985; 17 (12): 1173-83.

Gallup WD, Norris LC The essentialness of manganese for the normal development of bone. Science 1938; 87 (2245): 18-9.

Strause LG, Hegenauer J, Saltman P et al. Eff ects of long-term dietary manganese and copper defi ciency on rat skeleton. J Nutr 1986; 116 (1): 135-41.

Marrotte EJ, Chen DD, Hakim JS, Chen AF Manganese superoxide dis-mutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice. J Clin Invest 2010; 120 (12): 4207-19 doi.

Bolze MS, Reeves RD, Lindbeck FE et al. Infl uence of manganese on growth, somatomedin and glycosaminoglycan metabolism. J Nutr 1985; 115 (3): 352-8.

Leach RM, Muenster AM Studies on the role of manganese in bone formation. I. Eff ect upon the mucopolysaccharide content of chick bone. J Nutr 1962; 78:51-6.

Tal E, Guggenheim K Eff ect of manganese on calcifi cation of bone. BiochemJ1965; 95:94-7.

Henry PR, Ammerman CB, Littell RC Relative bioavailability of manganese from a manganese-methionine complex and inorganic sources for ruminants. J Dairy Sci 1992; 75 (12): 3473-8.

Izumikawa T, Kitagawa H Mice defi cient in glucuronyltransferase-I. Prog Mol Biol Transl Sci 2010;93:19-3450. Okajima T, Fukumoto S, Furukawa K Urano T. Molecular basis for the progeroid variant of Ehlers-Danlos syndrome. Identifi cation and characterization of two mutations in galactosyltransferase I gene. J Biol Chem 1999; 274 (41): 28841-4.

Sato T, Kudo T, Ikehara Y Chondroitin sulfate N-acetylgalactosaminyl-transferase 1 is necessary for normal endochondral ossifi cation and ag-grecan metabolism. J Biol Chem 2011; 286 (7): 5803-12.

Watanabe Y, Takeuchi K, Higa Onaga S et al. Chondroitin sulfate N-ace-tylgalactosaminyltransferase-1 is required for normal cartilage development. Biochem J 2010; 432 (1): 47-55.

Rodionova NA, Shabaeva KV Experience of the Tothema use in preoperative preparation in women with iron defi ciency anemia. Information Letter for Doctors. Perinatal Center of Ulyanovsk (Simbirsk), 2003.

Stucklov NI A meta-analysis of tolerability of drinking form of ferric gluconate (Fe2+), copper and manganese (Tothema) in the treatment of iron defi ciency anemia in children and adults. Country Doctor. 2012, 4 (15): 11-20.


GOST Style Citations


Нечаева Г.И., Яковлев В.М., Громова О.А. и др. Дисплазии соединительной ткани у детей и подростков. Инновационные стационар-сберегающие технологии диагностики и лечения в педиатрии. М.: Союз педиатров России, 2009.

Mikhailova AV, Smolenskii AV Clinicalfeatures and physicalfi tness parameters in athletes with cardiac connective tissue dysplasia syndrome. Klin Med (Mosk.) 2004; 82 (8): 44-8.

Zakhar’ian AL, Zakhar’ian EA The severity of varicose vein disease of the lower extremities in various degree of the connective tissue dysplasia syndrome. KlinKhir 2005; 8:42 -4.

Торшин И.Ю., Громова О.А. Молекулярные механизмы магния и дисплазии соединительной ткани. Рос. мед. журн. 2008:263-9.

Domnitskaia TM, D’iachenko AV, Kupriianova OO, Domnitskii MMV Clinical value of the use of magnesium orotate in adolescents with syndrome of cardiac connective tissue dysplasia. Kardiologiia 2005; 45 (3): 76-81.

Torshin IYu Bioinformatics in the post-genomic era: sensing the change from molecular genetics to personalized medicine. Nova Biomedical Books, NY, USA, 2009. In «Bioinformatics in the Post-GenomicEra» series.

Alberts B, Johnson A, LewisJ et al. Molecular Biology of the Cell, 4th edition, Garland Science, 2002.

Diaz-Castro J, Lopez-Frias MR, Campos MS et al. Severe nutritional iron-defi ciency anaemia has a negative eff ect on some bone turnover biomar-kers in rats. Eur JNutr 2011.

Fadda M, Zirattu G, Espa E, Orani GMorphological aspects of the synovial membrane and femoral epiphyseal cartilage in experimentally induced chronic anemia. Ital J Orthop Traumatol 1992; 18 (2): 271-7.

Jorgensen L, Skjelbakken T, Lochen ML et al. Anemia and the risk ofnon-vertebral fractures: the Tromso Study. Osteoporos Int 2010; 21 (10):1761-8

Chen Z, Thomson CA, Aickin M et al. The relationship between incidence of fractures and anemia in older multiethnic women. J Am Geriatr Soc 2010;58 (12): 2337-44 doi.

Abraham R, WaltonJ, Russell L et al. Dietary determinants of postmenopausal bone loss at the lumbar spine: a possible benefi cial eff ect of iron. Osteoporos Int 2006; 17 (8): 1165-73.

Goerss JB, Kim CH, Atkinson EJ et al. Risk of fractures in patients with pernicious anemia. J Bone Miner Res 1992; 7 (5): 573-9.

Smoliar VI Eff ect of iron-defi cient diets on the formation of bone tissue. VoprPitan 1984; (5): 55-915. Mamedov LA, Kosaganova NIu, Rikhireva GT et al. Changes in the content of transferrin, ceruloplasmin, iron, and copper in blood serum and granulation tissue in wound healing in an experiment. Patol Fiziol Eksp Ter 1988; 4:58-61.

O’Dell BL Roles for iron and copper in connective tissue biosynthesis. Philos TransR SocLondBBiolSci 1981; 294 (1071):91-104.

Yeowell HN, Walker LC Ehlers-Danlos syndrome type VI results from a nonsense mutation and a splice sitemediated exon-skipping mutation in the lysyl hydroxylase gene. ProcAssocAm Physicians 1997; 109 (4): 383-96.

Van der Slot AJ, Zuurmond AM et al. Identifi cation of PLOD2 as telopep-tide lysyl hydroxylase, an important enzyme in fi brosis. J Biol Chem 2003; 278 (42):40967-72.

Ha VT, Marshall MK, Elsas LJ et al. A patient with Ehlers-Danlos syndrome type VI is a compound heterozygote for mutations in the lysyl hydro-xylase gene. J Clin Invest 1994; 93 (4): 1716-21.

Cabral WA, Chang W, Barnes AM et al. Prolyl 3-hydroxylase 1 defi ciency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat Genet 2007; 39 (3): 359-65.

Yamasaki K, Hagiwara H Excess iron inhibits osteoblast metabolism. Toxicol Lett 2009; 191 (2-3): 211-5. Epub 2009

Giordano N, Vaccai D, Cintorino M et al. Histopathological study of iron deposit distribution in the rheumatoid synovium. Clin Exp Rheumatol 1991;9 (5):463-7.

Sindrilaru A, Peters T, Wieschalka S et al. An unrestrained proinfl amma-tory M1 macrophage population induced by iron impairs wound healing in humans and mice. J Clin Invest 2011; 121 (3): 985-97 doi.

Jacob AK, Hotchkiss RS, DeMeester SL et al. Endothelial cell apoptosis is accelerated by inorganic iron and heat via an oxygen radical dependent mechanism. Surgery 1997; 122 (2): 243-53.

Торшин И.Ю., Громова О.А., Хаджидис А.К. Систематический анализ молекулярных механизмов воздействия железа, меди, марганца в патогенезе железодефицитной анемии. Клин. фармакология. 2010; 3.

Branda SS, Yang ZY, Chew A, Isaya G Mitochondrial intermediate peptidase and the yeast frataxin homolog together maintain mitochondrial iron homeostasis in Saccharomyces cerevisiae. Hum Mol Genet 1999; 8 (6): 1099-110.

Reeves PG, DeMars LC Copper defi ciency reduces iron absorption and biological half-life in male rats. J Nutr2004; 134 (8): 1953-7.

Broker S, Meunier B, Rich P et al.MtDNA mutations associated with si-deroblastic anaemia cause a defect of mitochondrial cytochrome c oxi-dase. Eur J Biochem 1998; 258 (1): 132-8.

Bannister JV, Bannister WH, Rotilio G Aspects of the structure, function, and applications of superoxide dismutase. CRC Crit Rev Biochem 1987; 22 (2): 111-80.

Zhang CM, Chi X, Wang B et al. Downregulation of STEAP4, a highly-expressed TNF-alpha-inducible gene in adipose tissue, is associated with obesity in humans. Acta Pharmacol Sin 2008; 29 (5):587-92.

Borkow G, Gabbay J, Dardik R et al. Molecular mechanisms of enhanced wound healing by copper oxide-impregnated dressings. Wound Repair Regen 2010; 18 (2): 266-7532. Cangul IT, Gul NY, Topal A, Yilmaz R. Evaluation of the eff ects of topical tripeptide-copper complex and zinc oxide on open wound healing in rabbits. Vet Dermatol 2006; 17 (6): 417-23.

Sen CK, Khanna S, Venojarvi M et al. Copper-induced vascular endothelial growth factor expression and wound healing. Am J Physiol Heart Circ Physiol 2002; 282 (5): H1821-H1827.

Dickson KA, Kang DK, Kwon YS et al. Ribonuclease inhibitor regulates neovascularization by human angiogenin. Biochemistry 2009; 48 (18):3804-6.

La Mendola D, Magri A, Vagliasindi LI et al. Copper (II) complexformation with a linear peptide encompassing the putative cell binding site of angiogenin. Dalton Trans 2010; 39 (44): 10678-84.

Soncin F, Guitton JD, Cartwright T, Badet JInteraction of human angio-genin with copper modulates angiogenin binding to endothelial cells. Bio-chem BiophysRes Commun 1997; 236 (3): 604-10.

Lowe NM, Lowe NM, Fraser WD, Jackson MJ Is there a potential therapeutic value of copper and zinc for osteoporosis? Proc Nutr Soc 2002; 61 (2): 181-5.

Smoliar VI, Biniashevskii EV [Eff ect of copper defi ciency on growth and bone tissue formation]. Vopr Pitan 1988; (6): 28-32.

Jonas J, Burns J, Abel EW et al. Impaired mechanical strength of bone in experimental copper defi ciency. Ann Nutr Metab 1993; 37 (5): 245-52.

Opsahl W, Zeronian H, Ellison M et al. Role of copper in collagen cross-linking and its infl uence on selected mechanical properties of chick bone and tendon. JNutr 1982; 112 (4): 708-16.

Borg TK, Klevay LM, Gay RE et al. Alteration of the connective tissue network of striated muscle in copper defi cient rats. J Mol Cell Cardiol 1985; 17 (12): 1173-83.

Gallup WD, Norris LC The essentialness of manganese for the normal development of bone. Science 1938; 87 (2245): 18-9.

Strause LG, Hegenauer J, Saltman P et al. Eff ects of long-term dietary manganese and copper defi ciency on rat skeleton. J Nutr 1986; 116 (1): 135-41.

Marrotte EJ, Chen DD, Hakim JS, Chen AF Manganese superoxide dis-mutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice. J Clin Invest 2010; 120 (12): 4207-19 doi.

Bolze MS, Reeves RD, Lindbeck FE et al. Infl uence of manganese on growth, somatomedin and glycosaminoglycan metabolism. J Nutr 1985; 115 (3): 352-8.

Leach RM, Muenster AM Studies on the role of manganese in bone formation. I. Eff ect upon the mucopolysaccharide content of chick bone. J Nutr 1962; 78:51-6.

Tal E, Guggenheim K Eff ect of manganese on calcifi cation of bone. BiochemJ1965; 95:94-7.

Henry PR, Ammerman CB, Littell RC Relative bioavailability of manganese from a manganese-methionine complex and inorganic sources for ruminants. J Dairy Sci 1992; 75 (12): 3473-8.

Izumikawa T, Kitagawa H Mice defi cient in glucuronyltransferase-I. Prog Mol Biol Transl Sci 2010;93:19-3450. Okajima T, Fukumoto S, Furukawa K Urano T. Molecular basis for the progeroid variant of Ehlers-Danlos syndrome. Identifi cation and characterization of two mutations in galactosyltransferase I gene. J Biol Chem 1999; 274 (41): 28841-4.

Sato T, Kudo T, Ikehara Y Chondroitin sulfate N-acetylgalactosaminyl-transferase 1 is necessary for normal endochondral ossifi cation and ag-grecan metabolism. J Biol Chem 2011; 286 (7): 5803-12.

Watanabe Y, Takeuchi K, Higa Onaga S et al. Chondroitin sulfate N-ace-tylgalactosaminyltransferase-1 is required for normal cartilage development. Biochem J 2010; 432 (1): 47-55.

Родионова Н.А., Шабаева K.B. Опыт применения препарата Тотема при предоперационной подготовке у женщин с железодефицитной анемией. Информационное письмо для врачей. Перинатальный центр г. Ульяновск (Симбирск), 2003

Стуклов Н.И Мета-анализ переносимости питьевой формы глюконата железа (Fe2+), меди и марганца (препарат Тотема) при лечении железодефицитной анемии у детей и взрослых. Земский врач. 2012; 4 (15): 11-20.





DOI: https://doi.org/10.18370/2309-4117.2013.12.101-110

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