Mechanisms of hyperhomocysteinemia induced skeletal muscle myopathy after ischemia in the CBS−/+ mouse model

International Journal of Molecular Sciences

Volumn 16, Issue 1, 2015, Pages 1252-1265

  Veeranki, Sudhakar ^a   Tyagi, Suresh C ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

CBS; CSE; H2S; Homocysteine; Ischemia; MTHFR; Nitrotyrosylation; PGC 1 ; PPAR ; Skeletal muscle

Indexed keywords

5, 10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; GLUTATHIONE; HEME OXYGENASE 1; HOMOCYSTEINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; 3-NITROTYROSINE; ANTIOXIDANT; NITRIC OXIDE DONOR; PPARGC1A PROTEIN, MOUSE; PROTEIN BINDING; TRANSCRIPTION FACTOR; TYROSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CHEMICAL MODIFICATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; ISCHEMIA; MALE; METHYLATION; MOUSE; MYOPATHY; NITROTYROSYLATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN MODIFICATION; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; HYPERHOMOCYSTEINEMIA; METABOLISM; MUSCLE DISEASE; PATHOLOGY; VASCULARIZATION;

ANIMALS; ANTIOXIDANTS; BLOTTING, WESTERN; CYSTATHIONINE BETA-SYNTHASE; DISEASE MODELS, ANIMAL; HOMOCYSTEINE; HYPERHOMOCYSTEINEMIA; ISCHEMIA; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; MUSCULAR DISEASES; NITRIC OXIDE DONORS; PPAR GAMMA; PROTEIN BINDING; TRANSCRIPTION FACTORS; TYROSINE;

EID: 84920546326     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16011252     Document Type: Article

References (34)

1. Austin, R.C.; Lentz, S.R.; Werstuck, G.H. Role of hyperhomocysteinemia in endothelial dysfunction and atherothrombotic disease. Cell Death Differ. 2004, 11, S56-S64.
2. Mudd, S.H.; Finkelstein, J.D.; Irreverre, F.; Laster, L. Homocystinuria: An enzymatic defect. Science 1964, 143, 1443-1445.
3. Gibson, J.B.; Carson, N.A.; Neill, D.W. Pathological findings in homocystinuria. J. Clin. Pathol. 1964, 17, 427-437.
4. Thomas, P.S.; Carson, N.A. Homocystinuria. The evolution of skeletal changes in relation to treatment. Ann. Radiol. 1978, 21, 95-104.
5. Tamburrini, O.; Bartolomeo-de Iuri, A.; Andria, G.; Strisciuglio, P.; del Giudice, E.; Palescandolo, P.; Sartorio, R. Bone changes in homocystinuria in childhood. Radiol. Med. 1984, 70, 937-942.
6. Brosnan, J.T.; Jacobs, R.L.; Stead, L.M.; Brosnan, M.E. Methylation demand: A key determinant of homocysteine metabolism. Acta Biochim. Pol. 2004, 51, 405-413.
7. Robert, K.; Maurin, N.; Vayssettes, C.; Siauve, N.; Janel, N. Cystathionine beta synthase deficiency affects mouse endochondral ossification. Anat. Rec. A Discov. Mol. Cell. Evolut. Biol. 2005, 282, 1-7.
8. Holstein, J.H.; Herrmann, M.; Splett, C.; Herrmann, W.; Garcia, P.; Histing, T.; Klein, M.; Kurz, K.; Siebel, T.; Pohlemann, T. et al. High bone concentrations of homocysteine are associated with altered bone morphology in humans. Br. J. Nutr. 2011, 106, 378-382.
9. Kalra, B.R.; Ghose, S.; Sood, N.N. Homocystinuria with bilateral absolute glaucoma. Indian J. Ophthalmol. 1985, 33, 195-197.
10. Iacobazzi, V.; Infantino, V.; Castegna, A.; Andria, G. Hyperhomocysteinemia: Related genetic diseases and congenital defects, abnormal DNA methylation and newborn screening issues. Mol. Genet. Metab. 2014, 113, 27-33.
11. Veeranki, S.; Tyagi, S.C. Defective homocysteine metabolism: Potential implications for skeletal muscle malfunction. Int. J. Mol. Sci. 2013, 14, 15074-15091.
12. Narayanan, N.; Pushpakumar, S.B.; Givvimani, S.; Kundu, S.; Metreveli, N.; James, D.; Bratcher, A.P.; Tyagi, S.C. Epigenetic regulation of aortic remodeling in hyperhomocysteinemia. FASEB J. 2014, 28, 3411-3422.
13. Signorello, M.; Viviani, G.; Armani, U.; Cerone, R.; Minniti, G.; Piana, A.; Leoncini, G. Homocysteine, reactive oxygen species and nitric oxide in type 2 diabetes mellitus. Thromb. Res. 2007, 120, 607-613.
14. Neuman, J.C.; Albright, K.A.; Schalinske, K.L. Exercise prevents hyperhomocysteinemia in a dietary folate-restricted mouse model. Nutr. Res. 2013, 33, 487-493.
15. Van Guldener, C. Why is homocysteine elevated in renal failure and what can be expected from homocysteine-lowering? Nephrol. Dial. Transpl. 2006, 21, 1161-1166.
16. Sen, U.; Sathnur, P.B.; Kundu, S.; Givvimani, S.; Coley, D.M.; Mishra, P.K.; Qipshidze, N.; Tyagi, N.; Metreveli, N.; Tyagi, S.C. Increased endogenous H2S generation by cbs, cse, and 3mst gene therapy improves ex vivo renovascular relaxation in hyperhomocysteinemia. Am. J. Physiol. Cell Physiol. 2012, 303, C41-C51.
17. Ungvari, Z.; Csiszar, A.; Edwards, J.G.; Kaminski, P.M.; Wolin, M.S.; Kaley, G.; Koller, A. Increased superoxide production in coronary arteries in hyperhomocysteinemia—Role of tumor necrosis factor-alpha, nad(p)h oxidase, and inducible nitric oxide synthase. Arterioscler. Thromb. Vasc. 2003, 23, 418-424.
18. Faraci, F.M. Hyperhomocysteinemia—A million ways to lose control. Arterioscler. Thromb. Vasc. 2003, 23, 371-373.
19. Veeranki, S.; Givvimani, S.; Pushpakumar, S.; Tyagi, S.C. Hyperhomocysteinemia attenuates angiogenesis through reduction of hif-1alpha and pgc-1alpha levels in muscle fibers during hindlimb ischemia. Am. J. Physiol. Heart Circ. Physiol. 2014, 306, H1116-H1127.
20. Chintalgattu, V.; Harris, G.S.; Akula, S.A.; Katwa, L.C. Ppar-gamma agonists induce the expression of vegf and its receptors in cultured cardiac myofibroblasts. Cardiovasc. Res. 2007, 74, 140-150.
21. White, J.; Ruas, J.; Rao, R.; Kleiner, S.; Wu, J.; Spiegelman, B. A novel pgc-1a isoform induced by resistance training regulates skeletal muscle hypertrophy. FASEB J. 2013, 27, I8.
22. Handschin, C.; Choi, C.S.; Chin, S.; Kim, S.; Kawamori, D.; Kurpad, A.J.; Neubauer, N.; Hu, J.; Mootha, V.K.; Kim, Y.B. et al. Abnormal glucose homeostasis in skeletal muscle-specific pgc-1 alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk. J. Clin. Investig. 2007, 117, 3463-3474.
23. Sandri, M.; Lin, J.D.; Handschin, C.; Yang, W.L.; Arany, Z.P.; Lecker, S.H.; Goldberg, A.L.; Spiegelman, B.M. Pgc-1 alpha a protects skeletal muscle from atrophy by suppressing fox03 action and atrophy-specific gene transcription. Proc. Natl. Acad. Sci. USA 2006, 103, 16260-16265.
24. Rytinki, M.M.; Palvimo, J.J. Sumoylation attenuates the function of pgc-1alpha. J. Biol. Chem. 2009, 284, 26184-26193.
25. Jager, S.; Handschin, C.; Pierre, J.; Spiegelman, B.M. Amp-activated protein kinase (ampk) action in skeletal muscle via direct phosphorylation of pgc-1 alpha. Proc. Natl. Acad. Sci. USA 2007, 104, 12017-12022.
26. Li, X.H.; Monks, B.; Ge, Q.Y.; Birnbaum, M.J. Akt/pkb regulates hepatic metabolism by directly inhibiting pgc-1 alpha transcription coactivator. Nature 2007, 447, U1012-U1018.
27. Lee, M.H.; Jang, M.H.; Kim, E.K.; Han, S.W.; Cho, S.Y.; Kim, C.J. Nitric oxide induces apoptosis in mouse c2c12 myoblast cells. J. Pharmacol. Sci. 2005, 97, 369-376.
28. Kolling, J.; Scherer, E.B.; Siebert, C.; Marques, E.P.; dos Santos, T.M.; Wyse, A.T. Creatine prevents the imbalance of redox homeostasis caused by homocysteine in skeletal muscle of rats. Gene 2014, 545, 72-79.
29. Wei, H.L.; Zhang, C.Y.; Jin, H.F.; Tang, C.S.; Du, J.B. Hydrogen sulfide regulates lung tissue-oxidized glutathione and total antioxidant capacity in hypoxic pulmonary hypertensive rats. Acta Pharmacol. Sin. 2008, 29, 670-679.
30. Kundu, S.; Tyagi, N.; Sen, U.; Tyagi, S.C. Matrix imbalance by inducing expression of metalloproteinase and oxidative stress in cochlea of hyperhomocysteinemic mice. Mol. Cell. Biochem. 2009, 332, 215-224.
31. Hsieh, H.J.; Liu, C.A.; Huang, B.; Tseng, A.H.; Wang, D.L. Shear-induced endothelial mechanotransduction: The interplay between reactive oxygen species (ros) and nitric oxide (no) and the pathophysiological implications. J. Biomed. Sci. 2014, 21, 3.
32. Salom, M.G.; Arregui, B.; Carbonell, L.F.; Ruiz, F.; Gonzalez-Mora, J.L.; Fenoy, F.J. Renal ischemia induces an increase in nitric oxide levels from tissue stores. Am. J. Physiol. Reg. I 2005, 289, R1459-R1466.
33. Matsunaga, T.; Warltier, D.C.; Weihrauch, D.W.; Moniz, M.; Tessmer, J.; Chilian, W.M. Ischemia-induced coronary collateral growth is dependent on vascular endothelial growth factor and nitric oxide. Circulation 2000, 102, 3098-3103.
34. Watanabe, M.; Osada, J.; Aratani, Y.; Kluckman, K.; Reddick, R.; Malinow, M.R.; Maeda, N. Mice deficient in cystathionine beta-synthase—Animal-models for mild and severe homocyst(e)inemia. Proc. Natl. Acad. Sci. USA 1995, 92, 1585-1589.