Login Register Cart 0
Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Medical and Veterinary Importance of the Moonlighting Functions of Triosephosphate Isomerase

Author(s): Mónica Rodríguez-Bolaños and Ruy Perez-Montfort*

Volume 20, Issue 4, 2019

Page: [304 - 315] Pages: 12

DOI: 10.2174/1389203719666181026170751

Price: $65

Abstract

Triosephosphate isomerase is the fifth enzyme in glycolysis and its canonical function is the reversible isomerization of glyceraldehyde-3-phosphate and dihydroxyacetone phosphate. Within the last decade multiple other functions, that may not necessarily always involve catalysis, have been described. These include variations in the degree of its expression in many types of cancer and participation in the regulation of the cell cycle. Triosephosphate isomerase may function as an auto-antigen and in the evasion of the immune response, as a factor of virulence of some organisms, and also as an important allergen, mainly in a variety of seafoods. It is an important factor to consider in the cryopreservation of semen and seems to play a major role in some aspects of the development of Alzheimer's disease. It also seems to be responsible for neurodegenerative alterations in a few cases of human triosephosphate isomerase deficiency. Thus, triosephosphate isomerase is an excellent example of a moonlighting protein.

Keywords: Triosephosphate isomerase, moonlighting, cancer, antibody, virulence factor, allergen, cryopreservation, Alzheimer's disease, neurodegeneration.

« Previous Next »
Graphical Abstract

[1]
Katebi, A.R.; Jernigan, R.L. The critical role of the loops of triosephosphate isomerase for its oligomerization, dynamics, and functionality. Protein Sci., 2014, 23, 213-228.
[2]
Bar-Even, A.; Flamholz, A.; Noor, E.; Milo, R. Rethinking glycolysis: On the biochemical logic of metabolic pathways. Nat. Chem. Biol., 2012, 8, 509-517.
[3]
Osterman, A. Biogenesis and homeostasis of nicotinamide adenine dinucleotide cofactor. Ecosal Plus, 2009, 3
[http://dx.doi.org/10.1128/ ecosalplus.3.6.3.10]
[4]
Richard, J.P. Restoring a metabolic pathway. ACS Chem. Biol., 2008, 3, 605-607.
[5]
Lincet, H.; Icard, P. How do glycolytic enzymes favour cancer cell proliferation by nonmetabolic functions? Oncogene, 2015, 34, 3751-3759.
[6]
Roland, B.P.; Stuchul, K.A.; Larsen, S.B.; Amrich, C.G.; VanDemark, A.P.; Celotto, A.M.; Palladino, M.J. Evidence of a triosephosphate isomerase non-catalytic function crucial to behavior and longevity. J. Cell Sci., 2013, 126, 3151-3158.
[7]
Roland, B.P.; Zeccola, A.M.; Larsen, S.B.; Amrich, C.G.; Talsma, A.D.; Stuchul, K.A.; Heroux, A.; Levitan, E.S.; VanDemark, A.P.; Palladino, M.J. Structural and genetic studies demonstrate neurologic dysfunction in triosephosphate isomerase deficiency is associated with impaired synaptic vesicle dynamics. PLoS Genet., 2016, 12, e1005941.
[8]
Banner, D.W.; Bloomer, A.C.; Petsko, G.A.; Phillips, D.C.; Pogson, C.I.; Wilson, I.A.; Corran, P.H.; Furth, A.J.; Milman, J.D.; Offord, R.E.; Priddle, J.D.; Waley, S.G. Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 Å resolution: Using amino acid sequence data. Nature, 1975, 255, 609-614.
[9]
Lesk, A.M.; Brändén, C.I.; Chothia, C. Structural principles of α/β barrel proteins: the packing of the interior of the sheet. Proteins, 1989, 5, 139-148.
[10]
Wierenga, R.K. The TIM-barrel fold: A versatile framework for efficient enzymes. FEBS Lett., 2001, 492, 193-198.
[11]
Alber, T.; Banner, D.W.; Bloomer, A.C.; Petsko, G.A.; Phillips, D.; Rivers, P.S.; Wilson, I.A. On the three-dimensional structure and catalytic mechanism of triose phosphate isomerase. Philos. Trans. R. Soc. Lond. B Biol. Sci., 1981, 293, 159-171.
[12]
Wierenga, R.K.; Kapetaniou, E.G.; Venkatesan, R. Triosephosphate isomerase: A highly evolved biocatalyst. Cell. Mol. Life Sci., 2010, 67, 3961-3982.
[13]
Jeffery, C.J. Moonlighting proteins: old proteins learning new tricks. Trends Genet., 2003, 19, 415-417.
[14]
Dang, Y.; Wang, Z.; Guo, Y.; Yang, J.; Xing, Z.; Mu, L.; Zhang, X.; Ding, Z. Overexpression of triosephosphate isomerase inhibits proliferation of chicken embryonal fibroblast cells. Asian Pac. J. Cancer Prev., 2011, 12, 3479-3482.
[15]
Beranova-Giorgianni, S.; Zhao, Y.; Desiderio, D.M.; Giorgianni, F. Phosphoproteomic analysis of the human pituitary. Pituitary, 2006, 9, 109-120.
[16]
Dephoure, N.; Zhou, C.; Villén, J.; Beausoleil, S.A.; Bakalarski, C.E.; Elledge, S.J.; Gygi, S.P. A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA, 2008, 105, 10762-10767.
[17]
Imami, K.; Sugiyama, N.; Kyono, Y.; Tomita, M.; Ishihama, Y. Automated phosphoproteome analysis for cultured cancer cells by two-dimensional nanoLC-MS using a calcined titania / C18 biphasic column. Anal. Sci., 2008, 24, 161-166.
[18]
Pancholi, V.; Chhatwal, G.S. Housekeeping enzymes as virulence factors for pathogens. Int. J. Med. Microbiol., 2003, 293, 391-401.
[19]
Chuang, J.G.; Su, S.N.; Chiang, B.L.; Lee, H.J.; Chow, L.P. Proteome mining for novel IgE-binding proteins from the German cockroach (Blattella germanica) and allergen profiling of patients. Proteomics, 2010, 10, 3854-3867.
[20]
Vilagran, I.; Castillo, J.; Bonet, S.; Sancho, S.; Yeste, M.; Estanyol, J.M.; Oliva, R. Acrosin-binding protein (ACRBP) and triosephosphate isomerase (TPI) are good markers to predict boar sperm freezing capacity. Theriogenology, 2013, 80, 443-450.
[21]
Ahmed, N.; Battah, S.; Karachalias, N.; Babaei-Jadidi, R.; Horányi, M.; Baróti, K.; Hollan, S.; Thornalley, P.J. Increased formation of methylglyoxal and protein glycation, oxidation and nitrosation in triosephosphate isomerase deficiency. Biochim. Biophys. Acta, 2003, 1639, 121-132.
[22]
Schneider, A.S. Triosephosphate isomerase deficiency: Historical perspectives and molecular aspects. Best Pract. Res. Clin. Haematol., 2000, 13, 119-140.
[23]
Yang, F.; Xiao, Z.Q.; Zhang, X.Z.; Li, C.; Zhang, P.F.; Li, M.; Chen, Y.; Zhu, G.Q.; Sun, Y.; Liu, Y.F.; Chen, Z.C. Identification of tumor antigens in human lung squamous carcinoma by serological proteome analysis. J. Proteome Res., 2007, 6, 751-758.
[24]
Wang, X.; Lu, Y.; Yang, J.; Shi, Y.; Lan, M.; Liu, Z.; Zhai, H.; Fan, D. Identification of triosephosphate isomerase as an anti-drug resistance agent in human gastric cancer cells using functional proteomic analysis. J. Cancer Res. Clin. Oncol., 2008, 134, 995-1003.
[25]
Jiang, H.; Ma, N.; Shang, Y.; Zhou, W.; Chen, T.; Guan, D.; Li, J.; Wang, J.; Zhang, E.; Feng, Y.; Yin, F.; Yuan, Y.; Fang, Y.; Qiu, L.; Xie, D.; Wei, D. Triosephosphate isomerase 1 suppresses growth, migration and invasion of hepatocellular carcinoma cells. Biochem. Biophys. Res. Commun., 2017, 482, 1048-1053.
[26]
Chen, T.; Huang, Z.; Tian, Y.; Lin, B.; He, R.; Wang, H.; Ouyang, P.; Chen, H.; Wu, L. Clinical significance and prognostic value of triosephosphate isomerase expression in gastric cancer. Medicine (Baltimore), 2017, 96, e6865.
[27]
Chen, T.; Huang, Z.; Tian, Y.; Wang, H.; Ouyang, P.; Chen, H.; Wu, L.; Lin, B.; He, R. Role of triosephosphate isomerase and downstream functional genes on gastric cancer. Oncol. Rep., 2017, 38, 1822-1832.
[28]
Ford, H.L.; Pardee, A.B. Cancer and the cell cycle. J. Cell. Biochem., 1999, (Suppl. 32-33), 166-172
[29]
Zhu, J.; Xu, J.; Wang, Y.; Li, C.; Chen, Z.; Song, L.; Gao, J.; Yu, R. Purification and structural characterization of a novel-tumor protein from Arca inflata. Int. J. Biol. Macromol., 2017, 105, 103-110.
[30]
Toyama, A.; Suzuki, A.; Shimada, T.; Aoki, C.; Aoki, Y.; Umino, Y.; Nakamura, Y.; Aoki, D.; Sato, T.A. Proteomic characterization of ovarian cancers identifying annexin-A4, phosphoserine aminotransferase, cellular retinoic acid-binding protein 2, and serpin B5 as histology-specific biomarkers. Cancer Sci., 2012, 103, 747-755.
[31]
Paricharttanakul, N.M.; Saharat, K.; Chokchaichamnankit, D.; Punyarit, P.; Srisomsap, C.; Svasti, J. Unveiling a novel biomarker panel for diagnosis and classification of well-differentiated thyroid carcinomas. Oncol. Rep., 2016, 35, 2286-2296.
[32]
Desmetz, C.; Bibeau, F.; Boissière, F.; Bellet, V.; Rouanet, P.; Maudelonde, T.; Mangé, A.; Solassol, J. Proteomics-based identification of HSP60 as a tumor-associated antigen in early stage breast cancer and ductal carcinoma in situ. J. Proteome Res., 2008, 7, 3830-3837.
[33]
Zamani-Ahmadmahmudi, M.; Nassiri, S.M.; Rahbarghazi, R. Serological proteome analysis of dogs with breast cancer unveils common serum biomarkers with human counterparts. Electrophoresis, 2014, 35, 901-910.
[34]
Gao, H.; Zheng, Z.; Mao, Y.; Wang, W.; Qiao, Y.; Zhou, L.; Liu, F.; He, H.; Zhao, X. Identification of tumor antigens that elicit a humoral immune response in the sera of chinese esophageal squamous cell carcinoma patients by modified serological proteome analysis. Cancer Lett., 2014, 344, 54-61.
[35]
Valera, V.A.; Li-Ning, T.E.; Walter, B.A.; Roberts, D.D.; Linehan, W.M.; Merino, M.J. Protein expression profiling in the spectrum of renal cell carcinomas. J. Cancer, 2010, 1, 184-196.
[36]
Unwin, R.D.; Craven, R.A.; Harnden, P.; Hanrahan, S.; Totty, N.; Knowles, M.; Eardley, I.; Selby, P.J.; Banks, R.E. Proteomic changes in renal cancer and co-ordinate demonstration of both the glycolytic and mitochondrial aspects of the Warburg effect. Proteomics, 2003, 3, 1620-1632.
[37]
Wang, J.W.; Peng, S.Y.; Li, J.T.; Wang, Y.; Zhang, Z.P.; Cheng, Y.; Cheng, D.Q.; Weng, W.H.; Wu, X.S.; Fei, X.Z.; Quan, Z.W.; Li, Z.Y.; Li, S.G.; Liu, Y.B. Identification of metastasis-associated proteins involved in gallbladder carcinoma metastasis by proteomic analysis and functional exploration of chloride intracellular channel 1. Cancer Lett., 2009, 281, 71-81.
[38]
Yoshida, A.; Okamoto, N.; Tozawa-Ono, A.; Koizumi, H.; Kiguchi, K.; Ishizuka, B.; Kumai, T.; Suzuki, N. Proteomic analysis of differential protein expression by brain metastases of gynecological malignancies. Hum. Cell, 2013, 26, 56-66.
[39]
Hong, Y.; Huang, J. Autoantibodies against tumor-associated antigens for detection of hepatocellular carcinoma. World J. Hepatol., 2015, 7, 1581-1585.
[40]
Pieper, R.; Christian, R.E.; Gonzales, M.I.; Nishimura, M.I.; Gupta, G.; Settlage, R.E.; Shabanowitz, J.; Rosenberg, S.A.; Hunt, D.F.; Topalian, S.L. Biochemical identification of a mutated human melanoma antigen recognized by CD4(+) T cells. J. Exp. Med., 1999, 189, 757-766.
[41]
Sato, S.; Yashiro, M.; Asano, T.; Kobayashi, H.; Watanabe, H.; Migita, K. Association of anti-triosephosphate isomerase antibodies with aseptic meningitis in patients with neuropsychiatric systemic lupus erythematosus. Clin. Rheumatol., 2017, 36, 1655-1659.
[42]
Watanabe, H.; Seino, T.; Sato, Y. Antibodies to triosephosphate isomerase in patients with neuropsychiatric lupus. Biochem. Biophys. Res. Commun., 2004, 321, 949-953.
[43]
Sasajima, T.; Watanabe, H.; Sato, S.; Sato, Y.; Ohira, H. Anti-triosephosphate isomerase antibodies in cerebrospinal fluid are associated with neuropsychiatric lupus. J. Neuroimmunol., 2006, 181, 150-156.
[44]
Xiang, Y.; Sekine, T.; Nakamura, H.; Imajoh-Ohmi, S.; Fukuda, H.; Nishioka, K.; Kato, T. Proteomic surveillance of autoimmunity in osteoarthritis: identification of triosephosphate isomerase as an autoantigen in patients with osteoarthritis. Arthritis Rheum., 2004, 50, 1511-1521.
[45]
Ritter, S.; Schröder, S.; Uy, A.; Ritter, K. Haemolysis in hepatitis A virus infections coinciding with the occurrence of autoantibodies against triosephosphate isomerase and the reactivation of latent persistent Epstein-Barr virus infection. J. Med. Virol., 1996, 50, 272-275.
[46]
Kolln, J.; Ren, H.M.; Da, R.R.; Zhang, Y.; Spillner, E.; Olek, M.; Hermanowicz, N.; Hilgenberg, L.G.; Smith, M.A.; van den Noort, S.; Qin, Y. Triosephosphate isomerase- and glyceraldehyde-3-phosphate dehydrogenase-reactive autoantibodies in the cerebrospinal fluid of patients with multiple sclerosis. J. Immunol., 2006, 177, 5652-5658.
[47]
Furuya, H.; Ikeda, R. Interaction of triosephosphate isomerase from Staphylococcus aureus with plasminogen. Microbiol. Immunol., 2011, 55, 855-862.
[48]
Furuya, H.; Ikeda, R. Interaction of triosephosphate isomerase from the cell surface of Staphylococcus aureus and alpha-(1->3)-mannooligosaccharides derived from glucuronoxylomannan of Cryptococcus neoformans. Microbiology, 2009, 155, 2707-2713.
[49]
Ramiah, K.; van Reenen, C.A.; Dicks, L.M.T. Surface-bound proteins of Lactobacillus plantarum 423 that contribute to adhesion of Caco-2 cells and their role in competitive exclusion and displacement of Clostridium sporogenes and Enterococcus faecalis. Res. Microbiol., 2008, 159, 470-475.
[50]
Kinoshita, H.; Ohuchi, S.; Arakawa, K.; Watanabe, M.; Kitazawa, H.; Saito, T. Isolation of lactic acid bacteria bound to the porcine intestinal mucosa and an analysis of their moonlighting adhesins. Biosci. Microbiota Food Health, 2016, 35, 185-196.
[51]
Miranda-Ozuna, J.F.; Hernández-García, M.S.; Brieba, L.G.; Benítez-Cardoza, C.G.; Ortega-López, J.; González-Robles, A.; Arroyo, R. The glycolytic enzyme triosephosphate isomerase of Trichomonas vaginalis is a surface-associated protein induced by glucose that functions as a laminin- and fibronectin-binding protein. Infect. Immun., 2016, 84, 2878-2894.
[52]
Yamaguchi, M.; Ikeda, R.; Nishimura, M.; Kawamoto, S. Localization by scanning immunoelectron microscopy of triosephosphate isomerase, the molecules responsible for contact-mediated killing of Cryptococcus, on the surface of Staphylococcus. Microbiol. Immunol., 2010, 54, 368-370.
[53]
Ikeda, R.; Ichikawa, T. Interaction of surface molecules on Cryptococcus neoformans with plasminogen. FEMS Yeast Res., 2014, 14, 445-450.
[54]
Ditgen, D.; Anandarajah, E.M.; Meissner, K.A.; Brattig, N.; Wrenger, C.; Liebau, E. Harnessing the helminth secretome for therapeutic immunomodulators. BioMed Res. Int., 2014, 2014, 964350.
[55]
Bennuru, S.; Semnani, R.; Meng, Z.; Ribeiro, J.M.C.; Veenstra, T.D.; Nutman, T.B. Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Negl. Trop. Dis., 2009, 3, e410.
[56]
Hewitson, J.P.; Rückerl, D.; Harcus, Y.; Murray, J.; Webb, L.M.; Babayan, S.A.; Allen, J.E.; Kurniawan, A.; Maizels, R.M. The secreted triose phosphate isomerase of Brugia malayi is required to sustain microfilaria production in vivo. PLoS Pathog., 2014, 10, e1003930.
[57]
Liu, F.; Li, S.; Liu, G.; Li, F. Triosephosphate isomerase (TPI) facilitates the replication of WSSV in Exopalaemon carinicauda. Dev. Comp. Immunol., 2017, 71, 28-36.
[58]
Vester, D.; Rapp, E.; Kluge, S.; Genzel, Y.; Reichl, U. Virus-host cell interactions in vaccine production cell lines infected with different human influenza A virus variants: A proteomic approach. J. Proteomics, 2010, 73, 1656-1669.
[59]
Pastor, C.; Cuesta-Herranz, J.; Cases, B.; Pérez-Gordo, M.; Figueredo, E.; de las Heras, M.; Vivanco, F. Identification of major allergens in watermelon. Int. Arch. Allergy Immunol., 2009, 149, 291-298.
[60]
Yang, Y.; Chen, Z.W.; Hurlburt, B.K.; Li, G.L.; Zhang, Y.X.; Fei, D.X.; Shen, H.W.; Cao, M.J.; Liu, G.M. Identification of triosephosphate isomerase as a novel allergen in Octopus fangsiao. Mol. Immunol., 2017, 85, 35-46.
[61]
Hoppe, S.; Steinhart, H.; Paschke, A. Identification of a 28 kDa Lychee allergen as a triose-phosphate isomerase. Food Agric. Immunol., 2006, 17, 9-19.
[62]
Radauer, C.; Bublin, M.; Wagner, S.; Mari, A.; Breiteneder, H. Allergens are distributed into few protein families and possess a restricted number of biochemical functions. J. Allergy Clin. Immunol., 2008, 121, 847-852.
[63]
Hoffmann-Sommergruber, K.; Bruckmüller, M. Watermelon contains 92% water but it also contains allergens! Int. Arch. Allergy Immunol., 2009, 149, 289-290.
[64]
Kamath, S.D.; Rahman, A.M.; Voskamp, A.; Komoda, T.; Rolland, J.M.; O’Hehir, R.E.; Lopata, A.L. Effect of heat processing on antibody reactivity to allergen variants and fragments of black tiger prawn: A comprehensive allergenomic approach. Mol. Nutr. Food Res., 2014, 58, 1144-1155.
[65]
Yang, Y.; Zhang, Y.X.; Liu, M.; Maleki, S.J.; Zhang, M.L.; Liu, Q.M.; Cao, M.J.; Su, W.J.; Liu, G.M. Triosephosphate isomerase and Filamin C share common epitopes as novel allergens of Procambarus clarkii. J. Agric. Food Chem., 2017, 65, 950-963.
[66]
Chen, Y.H.; Lee, M.F.; Lan, J.L.; Chen, C.S.; Wang, H.L.; Hwang, G.Y.; Wu, C.H. Hypersensitivity to Forcipomyia taiwana (biting midge): Clinical analysis and identification of major For t 1, For t 2 and For t 3 allergens. Allergy, 2005, 60, 1518-1523.
[67]
Posch, A.; Chen, Z.; Wheeler, C.; Dunn, M.J.; Raulf-Heimsoth, M.; Baur, X. Characterization and identification of latex allergens by two-dimensional electrophoresis and protein microsequencing. J. Allergy Clin. Immunol., 1997, 99, 385-395.
[68]
Bauermeister, K.; Wangorsch, A.; Garoffo, L.P.; Reuter, A.; Conti, A.; Taylor, S.L.; Lidholm, J.; Dewitt, A.M.; Enrique, E.; Vieths, S.; Holzhauser, T.; Ballmer-Weber, B.; Reese, G. Generation of a comprehensive panel of crustacean allergens from the north sea shrimp Crangon crangon. Mol. Immunol., 2011, 48, 1983-1992.
[69]
Pérez-Gordo, M.; Pastor Vargas, C.; Cases, B.; De Las Heras, M.; Sanz, A.; Vivanco, F.; Cuesta-Herranz, J. New allergen involved in a case of allergy to Solea solea, common sole. Ann. Allergy Asthma Immunol., 2010, 104, 352-353.
[70]
He, R.; Zhang, H.; Shen, N.; Guo, C.; Ren, Y.; Xie, Y.; Gu, X.; Lai, W.; Peng, X.; Yang, G. Molecular characterization and allergenicity potential of triosephosphate isomerase from Sarcoptes scabiei. Vet. Parasitol., 2018, 257, 40-47.
[71]
Hauser, M.; Roulias, A.; Ferreira, F.; Egger, M. Panallergens and their impact on the allergic patient. Allergy Asthma Clin. Immunol., 2010, 6, 1.
[72]
Rosenberg, A.S. Effects of protein aggregates: an immunologic perspective. AAPS J., 2006, 8, E501-E507.
[73]
Mao, H.Y.; Cao, M.J.; Maleki, S.J.; Cai, Q.F.; Su, W.J.; Yang, Y.; Liu, G.M. Structural characterization and IgE epitope analysis of arginine kinase from Scylla paramamosain. Mol. Immunol., 2013, 56, 463-470.
[74]
Cheng, C.Y.; Chen, P.R.; Chen, C.J.; Wang, S.H.; Chen, C.F.; Lee, Y.P.; Huang, S.Y. Differential protein expression in chicken spermatozoa before and after freezing-thawing treatment. Anim. Reprod. Sci., 2015, 152, 99-107.
[75]
Mostek, A.; Dietrich, M.A.; Słowińska, M.; Ciereszko, A. Cryopreservation of bull semen is associated with carbonylation of sperm proteins. Theriogenology, 2017, 92, 95-102.
[76]
Zangbar, M.S.; Keshtgar, S.; Zolghadri, J.; Gharesi-Fard, B. Antisperm protein targets in azoospermia men. J. Hum. Reprod. Sci., 2016, 9, 47-52.
[77]
Vilagran, I.; Castillo-Martín, M.; Prieto-Martínez, N.; Bonet, S.; Yeste, M. Triosephosphate isomerase (TPI) and epididymal secretory glutathione peroxidase (GPX5) are markers for boar sperm quality. Anim. Reprod. Sci., 2016, 165, 22-30.
[78]
Bailey, J.L.; Tardif, S.; Dubé, C.; Beaulieu, M.; Reyes-Moreno, C.; Lefièvre, L.; Leclerc, P. Use of phosphoproteomics to study tyrosine kinase activity in capacitating boar sperm. kinase activity and capacitation. Theriogenology, 2005, 63, 599-614.
[79]
Bone, W.; Jones, A.R.; Morin, C.; Nieschlag, E.; Cooper, T.G. Susceptibility of glycolytic enzyme activity and motility of spermatozoa from rat, mouse, and human to inhibition by proven and putative chlorinated antifertility compounds in vitro. J. Androl., 2001, 22, 464-470.
[80]
Cormier, N.; Bailey, J.L. A differential mechanism is involved during heparin- and cryopreservation-induced capacitation of bovine spermatozoa. Biol. Reprod., 2003, 69, 177-185.
[81]
Pons-Rejraji, H.; Bailey, J.L.; Leclerc, P. Cryopreservation affects bovine sperm intracellular parameters associated with capacitation and acrosome exocytosis. Reprod. Fertil. Dev., 2009, 21, 525-537.
[82]
Nakamura, T.; Cho, D.H.; Lipton, S.A. Redox regulation of protein misfolding, mitochondrial dysfunction, synaptic damage, and cell death in neurodegenerative diseases. Exp. Neurol., 2012, 238, 12-21.
[83]
Nakamura, T.; Tu, S.; Akhtar, M.W.; Sunico, C.R.; Okamoto, S.; Lipton, S.A. Aberrant protein S-nitrosylation in neurodegenerative diseases. Neuron, 2013, 78, 596-614.
[84]
Zahid, S.; Khan, R.; Oellerich, M.; Ahmed, N.; Asif, A.R. Differential S-nitrosylation of proteins in Alzheimer’s disease. Neuroscience, 2014, 256, 126-136.
[85]
Park, S.A.; Park, H.W.; Kim, N.H.; Kim, Y.H.; Kwak, M.J.; Shin, J.S.; Kim, C.W. Effects of Tau on the activity of triose phosphate isomerase (TPI) in brain cells. Neurochem. Int., 2010, 56, 886-892.
[86]
Hu, H.; Tan, C.C.; Tan, L.; Yu, J.T. A mitocentric view of Alzheimer’s disease. Mol. Neurobiol., 2017, 54, 6046-6060.
[87]
Coma, M.; Guix, F.X.; Uribesalgo, I.; Espuña, G.; Solé, M.; Andreu, D.; Muñoz, F.J. Lack of oestrogen protection in amyloid-mediated endothelial damage due to protein nitrotyrosination. Brain, 2005, 128, 1613-1621.
[88]
Tajes, M.; Eraso-Pichot, A.; Rubio-Moscardó, F.; Guivernau, B.; Bosch-Morató, M.; Valls-Comamala, V.; Muñoz, F.J. Methylglyoxal reduces mitochondrial potential and activates Bax and caspase-3 in neurons: Implications for Alzheimer’s disease. Neurosci. Lett., 2014, 580, 78-82.
[89]
Roland, B.P.; Amrich, C.G.; Kammerer, C.J.; Stuchul, K.A.; Larsen, S.B.; Rode, S.; Aslam, A.A.; Heroux, A.; Wetzel, R.; VanDemark, A.P.; Palladino, M.J. Triosephosphate isomerase I170V alters catalytic site, enhances stability and induces pathology in a Drosophila model of TPI deficiency. Biochim. Biophys. Acta, 2015, 1852, 61-69.
[90]
Guix, F.X.; Ill-Raga, G.; Bravo, R.; Nakaya, T.; de Fabritiis, G.; Coma, M.; Miscione, G.P.; Villà-Freixa, J.; Suzuki, T.; Fernández-Busquets, X.; Valverde, M.A.; de Strooper, B.; Muñoz, F.J. Amyloid-dependent triosephosphate isomerase nitrotyrosination induces glycation and tau fibrillation. Brain, 2009, 132, 1335-1345.
[91]
Knowles, J.R. Enzyme catalysis: Not different, just better. Nature, 1991, 350, 121-124.
[92]
Rozovsky, S.; McDermott, A.E. The time scale of the catalytic loop motion in triosephosphate isomerase. J. Mol. Biol., 2001, 310, 259-270.
[93]
Gao, W.; Zhao, J.; Li, H.; Gao, Z. Triosephosphate isomerase tyrosine nitration induced by heme – NaNO2 – H2 O2 or peroxynitrite : effects of different natural phenolic compounds. J. Biochem. Mol. Toxicol., 2017, 31
[http://dx.doi.org/10.1002/jbt.21893]
[94]
Ill-Raga, G.; Ramos-Fernández, E.; Guix, F.X.; Tajes, M.; Bosch-Morató, M.; Palomer, E.; Godoy, J.; Belmar, S.; Cerpa, W.; Simpkins, J.W.; Inestrosa, N.C.; Muñoz, F.J. Amyloid-β peptide fibrils induce nitro-oxidative stress in neuronal cells. J. Alzheimers Dis., 2010, 22, 641-652.
[95]
Kim, C.; Lim, Y.; Yoo, B.C.; Won, N.H.; Kim, S.; Kim, G. Regulation of post-translational protein arginine methylation during HeLa cell cycle. Biochim. Biophys. Acta, 2010, 1800, 977-985.
[96]
Lee, W.H.; Choi, J.S.; Byun, M.R.; Koo, K.T.; Shin, S.; Lee, S.K.; Surh, Y.J. Functional inactivation of triosephosphate isomerase through phosphorylation during etoposide-induced apoptosis in HeLa cells: Potential role of Cdk2. Toxicology, 2010, 278, 224-228.
[97]
Sultana, R.; Butterfield, D.A. Identification of the oxidative stress proteome in the brain. Free Radic. Biol. Med., 2011, 50, 487-494.
[98]
Contreras, C.F.; Canales, M.A.; Alvarez, A.; Ferrari, G.V.; Inestrosa, N.C. Molecular modeling of the amyloid- beta -peptide using the homology to a fragment of triosephosphate isomerase that forms amyloid in vitro. Protein Eng., 1999, 12, 959-966.
[99]
Butterfield, D.A. Proteomics: A new approach to investigate oxidative stress in Alzheimer’s disease brain. Brain Res., 2004, 1000, 1-7.
[100]
Ralser, M.; Heeren, G.; Breitenbach, M.; Lehrach, H.; Krobitsch, S. Triose phosphate isomerase deficiency is caused by altered dimerization--not catalytic inactivity--of the mutant enzymes. PLoS One, 2006, 1, e30.
[101]
Orosz, F.; Oláh, J.; Ovádi, J. Triosephosphate isomerase deficiency: Facts and doubts. IUBMB Life, 2006, 58, 703-715.
[102]
Orosz, F.; Oláh, J.; Ovádi, J. Reappraisal of the triosephosphate isomerase deficiency. Eur. J. Haematol., 2011, 86, 265-267.
[103]
Serdaroglu, G.; Aydinok, Y.; Yilmaz, S.; Manco, L.; Özer, E. Triosephosphate isomerase deficiency: A patient with Val231Met mutation. Pediatr. Neurol., 2011, 44, 139-142.
[104]
Cabrera, N.; Torres-Larios, A.; García-Torres, I.; Enríquez-Flores, S.; Perez-Montfort, R. Differential effects on enzyme stability and kinetic parameters of mutants related to human triosephosphate isomerase deficiency. Biochim. Biophys. Acta, 2018, 1862, 1401-1409.
[105]
Hollán, S.; Magócsi, M.; Fodor, E.; Horányi, M.; Harsányi, V.; Farkas, T. Search for the pathogenesis of the differing phenotype in two compound heterozygote Hungarian brothers with the same genotypic triosephosphate isomerase deficiency. Proc. Natl. Acad. Sci. USA, 1997, 94, 10362-10366.
[106]
Hollán, S.; Dey, I.; Szollár, L.; Horányi, M.; Magócsi, M.; Harsányi, V.; Farkas, T. Erythrocyte lipids in triose-phosphate isomerase deficiency. Proc. Natl. Acad. Sci. USA, 1995, 92, 268-271.
[107]
Rodríguez-Almazán, C.; Arreola, R.; Rodríguez-Larrea, D.; Aguirre-López, B.; de Gómez-Puyou, M.T.; Pérez-Montfort, R.; Costas, M.; Gómez-Puyou, A.; Torres-Larios, A. Structural basis of human triosephosphate isomerase deficiency: mutation E104D is related to alterations of a conserved water network at the dimer interface. J. Biol. Chem., 2008, 283, 23254-23263.
[108]
Görlich, A.; Wolf, M.; Zimmermann, A.M.; Gurniak, C.B.; Al Banchaabouchi, M.; Sassoè-Pognetto, M.; Witke, W.; Friauf, E.; Rust, M.B. N- cofilin can compensate for the loss of ADF in excitatory synapses. PLoS One, 2011, 6, e26789.
[109]
Wolf, M.; Zimmermann, A.M.; Görlich, A.; Gurniak, C.B.; Sassoè-Pognetto, M.; Friauf, E.; Witke, W.; Rust, M.B. ADF/Cofilin controls synaptic actin dynamics and regulates synaptic vesicle mobilization and exocytosis. Cereb. Cortex, 2015, 25, 2863-2875.
[110]
Jung, J.; Yoon, T.; Choi, E.C.; Lee, K. Interaction of cofilin with triose-phosphate isomerase contributes glycolytic fuel for Na,K-ATPase via Rho-mediated signaling pathway. J. Biol. Chem., 2002, 277, 48931-48937.
[111]
Knull, H.R.; Walsh, J.L. Association of glycolytic enzymes with the cytoskeleton. Curr. Top. Cell. Regul., 1992, 33, 15-30.
[112]
Chen, G.; Gharib, T.G.; Huang, C.C.; Thomas, D.G.; Shedden, K.A.; Taylor, J.M.; Kardia, S.L.; Misek, D.E.; Giordano, T.J.; Iannettoni, M.D.; Orringer, M.B.; Hanash, S.M.; Beer, D.G. Proteomic analysis of lung adenocarcinoma: Identification of a highly expressed set of proteins in tumors. Clin. Cancer Res., 2002, 8, 2298-2305.
[113]
Wawrzyniak, M.; O’Mahony, L.; Akdis, M. Role of regulatory cells in oral tolerance. Allergy Asthma Immunol. Res., 2017, 9, 107-115.

Rights & Permissions Print Cite
Article Metrics
50
6
World Immunization Week
© 2024 Bentham Science Publishers | Privacy Policy