Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Thymosin β4: A Multi-Faceted Tissue Repair Stimulating Protein in Heart Injury

Author(s): Geir Bjørklund*, Maryam Dadar, Jan Aaseth and Salvatore Chirumbolo

Volume 27, Issue 37, 2020

Page: [6294 - 6305] Pages: 12

DOI: 10.2174/0929867326666190716125456

Price: $65

Abstract

Thymosin Beta-4 (Tβ4) is known as a major pleiotropic actin-sequestering protein that is involved in tumorigenesis. Tβ4 is a water-soluble protein that has different promising clinical applications in the remodeling and ulcerated tissues repair following myocardial infarction, stroke, plasticity and neurovascular remodeling of the Peripheral Nervous System (PNS) and the Central Nervous System (CNS). On the other hand, similar effects have been observed for Tβ4 in other kinds of tissues, including cardiac muscle tissue. In recent reports, as it activates resident epicardial progenitor cells and modulates inflammatory-caused injuries, Tβ4 has been suggested as a promoter of the survival of cardiomyocytes. Furthermore, Tβ4 may act in skeletal muscle and different organs in association/synergism with numerous other tissue repair stimulating factors, including melatonin and C-fiber-derived peptides. For these reasons, the present review highlights the promising role of Tβ4 in cardiac healing.

Keywords: Tissue repair, thymosin beta 4, melatonin, C-fiber-derived peptides, Peripheral Nervous System, Central Nervous System.

[1]
Goldstein, A.L.; Hannappel, E.; Kleinman, H.K. Thymosin β4: actin-sequestering protein moonlights to repair injured tissues. Trends Mol. Med., 2005, 11(9), 421-429.
[http://dx.doi.org/10.1016/j.molmed.2005.07.004 ] [PMID: 16099219]
[2]
Bokor, M.; Tantos, Á.; Mészáros, A.; Jenei, B.; Haminda, R.; Tompa, P.; Tompa, K. Molecular motions and interactions in aqueous solutions of Thymosin-β4, Stabilin C-Terminal Domain (CTD) and their 1:1 complex studied by 1H NMR spectroscopy. ChemPhysChem, 2018, 19(7), 848-856.
[http://dx.doi.org/10.1002/cphc.201701187 ] [PMID: 29274195]
[3]
Sosne, G.; Christopherson, P.L.; Barrett, R.P.; Fridman, R. Thymosin-β4 modulates corneal matrix metalloproteinase levels and polymorphonuclear cell infiltration after alkali injury. Invest. Ophthalmol. Vis. Sci., 2005, 46(7), 2388-2395.
[http://dx.doi.org/10.1167/iovs.04-1368 ] [PMID: 15980226]
[4]
Kumar, N.; Nakagawa, P.; Janic, B.; Romero, C.A.; Worou, M.E.; Monu, S.R.; Peterson, E.L.; Shaw, J.; Valeriote, F.; Ongeri, E.M.; Niyitegeka, J.M.; Rhaleb, N.E.; Carretero, O.A. The anti-inflammatory peptide Ac-SDKP is released from thymosin-β4 by renal meprin-α and prolyl oligopeptidase. Am. J. Physiol. Renal Physiol., 2016, 310(10), F1026-F1034.
[http://dx.doi.org/10.1152/ajprenal.00562.2015 ] [PMID: 26962108]
[5]
Sosne, G.; Szliter, E.A.; Barrett, R.; Kernacki, K.A.; Kleinman, H.; Hazlett, L.D. Thymosin beta 4 promotes corneal wound healing and decreases inflammation in vivo following alkali injury. Exp. Eye Res., 2002, 74(2), 293-299.
[http://dx.doi.org/10.1006/exer.2001.1125 ] [PMID: 11950239]
[6]
Sosne, G.; Qiu, P.; Goldstein, A.L.; Wheater, M. Biological activities of thymosin β4 defined by active sites in short peptide sequences. FASEB J., 2010, 24(7), 2144-2151.
[http://dx.doi.org/10.1096/fj.09-142307 ] [PMID: 20179146]
[7]
Choi, B.D.; Lim, H.J.; Lee, S.Y.; Lee, M.H.; Kil, K.S.; Lim, D.S.; Jeong, S.J.; Jeong, M.J. Thymosin β4 is associated with bone sialoprotein expression via ERK and Smad3 signaling pathways in MDPC-23 odontoblastic cells. Int. J. Mol. Med., 2018, 42(5), 2881-2890.
[http://dx.doi.org/10.3892/ijmm.2018.3865 ] [PMID: 30226623]
[8]
Osei, J.; Kelly, W.; Toffolo, K.; Donahue, K.; Levy, B.; Bard, J.; Wang, J.; Levy, E.; Nowak, N.; Poulsen, D. Thymosin beta 4 induces significant changes in the plasma miRNA profile following severe traumatic brain injury in the rat lateral fluid percussion injury model. Expert Opin. Biol. Ther., 2018, 18(sup1), 159-164.
[http://dx.doi.org/10.1080/14712598.2018.1484102] [PMID: 29873258]
[9]
Kim, J.H.; Jung, Y.; Kim, B-S.; Kim, S.H. Stem cell recruitment and angiogenesis of neuropeptide substance P coupled with self-assembling peptide nanofiber in a mouse hind limb ischemia model. Biomaterials, 2013, 34(6), 1657-1668.
[http://dx.doi.org/10.1016/j.biomaterials.2012.11.008 ] [PMID: 23206876]
[10]
Lee, S-I.; Lee, D-W.; Yun, H-M.; Cha, H-J.; Bae, C-H.; Cho, E-S.; Kim, E-C. Expression of thymosin beta-4 in human periodontal ligament cells and mouse periodontal tissue and its role in osteoblastic/cementoblastic differentiation. Differentiation, 2015, 90(1-3), 16-26.
[http://dx.doi.org/10.1016/j.diff.2015.08.003 ] [PMID: 26361868]
[11]
Cavasin, M.A. Therapeutic potential of thymosin-β4 and its derivative N-acetyl-seryl-aspartyl-lysyl-proline (Ac-SDKP) in cardiac healing after infarction. Am. J. Cardiovasc. Drugs, 2006, 6(5), 305-311.
[http://dx.doi.org/10.2165/00129784-200606050-00003 ] [PMID: 17083265]
[12]
Xiong, Y.; Mahmood, A.; Meng, Y.; Zhang, Y.; Zhang, Z.G.; Morris, D.C.; Chopp, M. Treatment of traumatic brain injury with thymosin β4 in rats. J. Neurosurg., 2011, 114(1), 102-115.
[http://dx.doi.org/10.3171/2010.4.JNS10118 ] [PMID: 20486893]
[13]
Zhang, Y.; Zhang, Z.G.; Chopp, M.; Meng, Y.; Zhang, L.; Mahmood, A.; Xiong, Y. Treatment of traumatic brain injury in rats with N-acetyl-seryl-aspartyl-lysyl-proline. J. Neurosurg., 2017, 126(3), 782-795.
[http://dx.doi.org/10.3171/2016.3.JNS152699 ] [PMID: 28245754]
[14]
Dubé, K.N.; Bollini, S.; Smart, N.; Riley, P.R. Thymosin β4 protein therapy for cardiac repair. Curr. Pharm. Des., 2012, 18(6), 799-806.
[http://dx.doi.org/10.2174/138161212799277699 ] [PMID: 22236126]
[15]
Kassem, K.M.; Vaid, S.; Peng, H.; Sarkar, S.; Rhaleb, N-E. Thymosinβ4-Ac-SDKP pathway: Any relevance for the cardiovascular system? Can. J. Physiol. Pharmacol., 2019.
[http://dx.doi.org/10.1139/cjpp-2018-0570]
[16]
Gao, X.Y.; Hou, F.; Zhang, Z.P.; Nuo, M.T.; Liang, H.; Cang, M.; Wang, Z.G.; Wang, X.; Xu, T.; Yan, L.Y.; Guo, X.D.; Liu, D.J. Role of thymosin beta 4 in hair growth. Mol. Genet. Genomics, 2016, 291(4), 1639-1646.
[http://dx.doi.org/10.1007/s00438-016-1207-y ] [PMID: 27130465]
[17]
Philp, D.; Badamchian, M.; Scheremeta, B.; Nguyen, M.; Goldstein, A.L.; Kleinman, H.K. Thymosin β 4 and a synthetic peptide containing its actin-binding domain promote dermal wound repair in db/db diabetic mice and in aged mice. Wound Repair Regen., 2003, 11(1), 19-24.
[http://dx.doi.org/10.1046/j.1524-475X.2003.11105.x ] [PMID: 12581423]
[18]
Philp, D.; Nguyen, M.; Scheremeta, B.; St-Surin, S.; Villa, A.M.; Orgel, A.; Kleinman, H.K.; Elkin, M. Thymosin β4 increases hair growth by activation of hair follicle stem cells. FASEB J., 2004, 18(2), 385-387.
[http://dx.doi.org/10.1096/fj.03-0244fje ] [PMID: 14657002]
[19]
Chopp, M.; Zhang, Z.G. Thymosin β4 as a restorative/regenerative therapy for neurological injury and neurodegenerative diseases. Exp. Opin. Biol. Ther., 2015, 15(Suppl. 1), 9-12.
[http://dx.doi.org/10.1517/14712598.2015.1005596]
[20]
Morris, D.C.; Chopp, M.; Zhang, L.; Zhang, Z.G. Thymosin β4: a candidate for treatment of stroke? Ann. N. Y. Acad. Sci., 2010, 1194(1), 112-117.
[http://dx.doi.org/10.1111/j.1749-6632.2010.05469.x ] [PMID: 20536457]
[21]
Gómez-Márquez, J. Function of prothymosin α in chromatin decondensation and expression of thymosin β-4 linked to angiogenesis and synaptic plasticity. Ann. N. Y. Acad. Sci., 2007, 1112(1), 201-209.
[http://dx.doi.org/10.1196/annals.1415.020 ] [PMID: 17495247]
[22]
Ramírez-Fernández, M.P.; Calvo-Guirado, J.L.; de-Val, J.E-M.S.; Delgado-Ruiz, R.A.; Negri, B.; Pardo-Zamora, G.; Peñarrocha, D.; Barona, C.; Granero, J.M.; Alcaraz-Baños, M. Melatonin promotes angiogenesis during repair of bone defects: a radiological and histomorphometric study in rabbit tibiae. Clin. Oral Investig., 2013, 17(1), 147-158.
[http://dx.doi.org/10.1007/s00784-012-0684-6 ] [PMID: 22323056]
[23]
Calvo-Guirado, J.L.; Ramírez-Fernández, M.P.; Gómez-Moreno, G.; Maté-Sánchez, J.E.; Delgado-Ruiz, R.; Guardia, J.; López-Marí, L.; Barone, A.; Ortiz-Ruiz, A.J.; Martínez-González, J.M.; Bravo, L.A. Melatonin stimulates the growth of new bone around implants in the tibia of rabbits. J. Pineal Res., 2010, 49(4), 356-363.
[http://dx.doi.org/10.1111/j.1600-079X.2010.00801.x ] [PMID: 20666975]
[24]
Galano, A.; Medina, M.E.; Tan, D.X.; Reiter, R.J. Melatonin and its metabolites as copper chelating agents and their role in inhibiting oxidative stress: a physicochemical analysis. J. Pineal Res., 2015, 58(1), 107-116.
[http://dx.doi.org/10.1111/jpi.12196 ] [PMID: 25424557]
[25]
Şener, G.; Toklu, H.; Kapucu, C.; Ercan, F.; Erkanli, G.; Kaçmaz, A.; Tilki, M.; Yeğen, B.Ç. Melatonin protects against oxidative organ injury in a rat model of sepsis. Surg. Today, 2005, 35(1), 52-59.
[http://dx.doi.org/10.1007/s00595-004-2879-1 ] [PMID: 15622465]
[26]
Sobhani, R.; Masoudpour, H.; Akbari, M.; Suzangar, H.R. AleSaeidio, S.; Adibi, S.; Khademi, S.A.; Khademi, E.F.; Sobhani, F. The histobiochemical effects of melatonin on ischemia reperfusion-related injuries in vascular trauma of lower limbs. Ann. Ital. Chir., 2012, 83(1), 49-54.
[PMID: 22352217]
[27]
Hibaoui, Y.; Roulet, E.; Ruegg, U.T. Melatonin prevents oxidative stress-mediated mitochondrial permeability transition and death in skeletal muscle cells. J. Pineal Res., 2009, 47(3), 238-252.
[http://dx.doi.org/10.1111/j.1600-079X.2009.00707.x ] [PMID: 19664004]
[28]
Rodriguez, M.I.; Escames, G.; López, L.C.; García, J.A.; Ortiz, F.; López, A.; Acuña-Castroviejo, D. Melatonin administration prevents cardiac and diaphragmatic mitochondrial oxidative damage in senescence-accelerated mice. J. Endocrinol., 2007, 194(3), 637-643.
[http://dx.doi.org/10.1677/JOE-07-0260 ] [PMID: 17761903]
[29]
Gonzalez-Candia, A.; Veliz, M.; Carrasco-Pozo, C.; Castillo, R.L.; Cárdenas, J.C.; Ebensperger, G.; Reyes, R.V.; Llanos, A.J.; Herrera, E.A. Antenatal melatonin modulates an enhanced antioxidant/pro-oxidant ratio in pulmonary hypertensive newborn sheep. Redox Biol., 2019, 22, 101128.
[http://dx.doi.org/10.1016/j.redox.2019.101128 ] [PMID: 30771751]
[30]
Mansouri, A.; Demeilliers, C.; Amsellem, S.; Pessayre, D.; Fromenty, B. Acute ethanol administration oxidatively damages and depletes mitochondrial DNA in mouse liver, brain, heart, and skeletal muscles: protective effects of antioxidants. J. Pharmacol. Exp. Ther., 2001, 298(2), 737-743.
[PMID: 11454938]
[31]
Anderson, G. Linking the biological underpinnings of depression: Role of mitochondria interactions with melatonin, inflammation, sirtuins, tryptophan catabolites, DNA repair and oxidative and nitrosative stress, with consequences for classification and cognition. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2018, 80(Pt C), 255-266.
[http://dx.doi.org/10.1016/j.pnpbp.2017.04.022 ] [PMID: 28433458]
[32]
Öner, J.; Öner, H.; Sahin, Z.; Demir, R.; Ustünel, I. Melatonin is as effective as testosterone in the prevention of soleus muscle atrophy induced by castration in rats. Anat. Rec. (Hoboken), 2008, 291(4), 448-455.
[http://dx.doi.org/10.1002/ar.20659 ] [PMID: 18293375]
[33]
Batmanabane, M. Melatonin is responsible for the nocturnal increase observed in serum and thymus of alpha1-thymosin and thymulin concentrations: observations in rats and humans. J. Neuroimmunol., 2007, 183(1-2), 239.
[http://dx.doi.org/10.1016/j.jneuroim.2006.10.012 ] [PMID: 17125848]
[34]
Weller, F.E.; Shah, U.; Cummings, G.D.; Chretien, P.B.; Mutchnick, M.G. Serum levels of immunoreactive thymosin alpha 1 and thymosin beta 4 in large cohorts of healthy adults. Thymus, 1992, 19(1), 45-52.
[PMID: 1566283]
[35]
Tang, M.C.; Su, Y. Thymosin β4 knockdown disrupts mitochondrial functions of SW480 human colon cancer cells. Cancer Sci., 2011, 102(9), 1665-1672.
[http://dx.doi.org/10.1111/j.1349-7006.2011.02002.x ] [PMID: 21668580]
[36]
Lopez-Gonzalez, M.A.; Guerrero, J.M.; Sanchez, B.; Delgado, F. Melatonin restores and enhances the human type B tonsillar lymphocyte subset in recurrent acute tonsillitis. Neurosci. Lett., 1998, 247(2-3), 131-134.
[http://dx.doi.org/10.1016/S0304-3940(98)00292-4 ] [PMID: 9655610]
[37]
Tan, D-X.; Reiter, R.J. Mitochondria: the birth place, battle ground and the site of melatonin metabolism in cells. Melatonin Research, 2019, 2(1), 44-66.
[http://dx.doi.org/10.32794/mr11250011]
[38]
Escames, G.; López, L.C.; Ortiz, F.; López, A.; García, J.A.; Ros, E.; Acuña-Castroviejo, D. Attenuation of cardiac mitochondrial dysfunction by melatonin in septic mice. FEBS J., 2007, 274(8), 2135-2147.
[http://dx.doi.org/10.1111/j.1742-4658.2007.05755.x ] [PMID: 17371545]
[39]
Pan, P.; Zhang, H.; Su, L.; Wang, X.; Liu, D. Melatonin balance the autophagy and apoptosis by regulating UCP2 in the LPS-induced cardiomyopathy. Molecules, 2018, 23(3), 675.
[http://dx.doi.org/10.3390/molecules23030675 ] [PMID: 29547569]
[40]
López, L.C.; Escames, G.; Ortiz, F.; Ros, E.; Acuña-Castroviejo, D. Melatonin restores the mitochondrial production of ATP in septic mice. Neuroendocrinol. Lett., 2006, 27(5), 623-630.
[PMID: 17159820]
[41]
Chahbouni, M.; Escames, G.; López, L.C.; Sevilla, B.; Doerrier, C.; Muñoz-Hoyos, A.; Molina-Carballo, A.; Acuña-Castroviejo, D. Melatonin treatment counteracts the hyperoxidative status in erythrocytes of patients suffering from Duchenne muscular dystrophy. Clin. Biochem., 2011, 44(10-11), 853-858.
[http://dx.doi.org/10.1016/j.clinbiochem.2011.04.001 ] [PMID: 21515247]
[42]
Chahbouni, M.; Escames, G.; Venegas, C.; Sevilla, B.; García, J.A.; López, L.C.; Muñoz-Hoyos, A.; Molina-Carballo, A.; Acuña-Castroviejo, D. Melatonin treatment normalizes plasma pro-inflammatory cytokines and nitrosative/oxidative stress in patients suffering from Duchenne muscular dystrophy. J. Pineal Res., 2010, 48(3), 282-289.
[http://dx.doi.org/10.1111/j.1600-079X.2010.00752.x ] [PMID: 20210854]
[43]
Spurney, C.F.; Cha, H-J.; Sali, A.; Pandey, G.S.; Pistilli, E.; Guerron, A.D.; Gordish-Dressman, H.; Hoffman, E.P.; Nagaraju, K. Evaluation of skeletal and cardiac muscle function after chronic administration of thymosin β-4 in the dystrophin deficient mouse. PLoS One, 2010, 5(1), e8976.
[http://dx.doi.org/10.1371/journal.pone.0008976 ] [PMID: 20126456]
[44]
Stratos, I.; Richter, N.; Rotter, R.; Li, Z.; Zechner, D.; Mittlmeier, T.; Vollmar, B. Melatonin restores muscle regeneration and enhances muscle function after crush injury in rats. J. Pineal Res., 2012, 52(1), 62-70.
[http://dx.doi.org/10.1111/j.1600-079X.2011.00919.x ] [PMID: 21790777]
[45]
Maarman, G.J.; Reiter, R.J. Melatonin therapy for blunt trauma and strenuous exercise: A mechanism involving cytokines, NFκB, Akt, MAFBX and MURF-1. J. Sports Sci., 2018, 36(16), 1897-1901.
[http://dx.doi.org/10.1080/02640414.2018.1424491 ] [PMID: 29313427]
[46]
Lissoni, P. Biochemotherapy with standard chemotherapies plus the pineal hormone melatonin in the treatment of advanced solid neoplasms. Pathol. Biol. (Paris), 2007, 55(3-4), 201-204.
[http://dx.doi.org/10.1016/j.patbio.2006.12.025 ] [PMID: 17446010]
[47]
Vigoré, L.; Messina, G.; Brivio, F.; Fumagalli, L.; Rovelli, F.DI; Fede, G.; Lissoni, P. Psychoneuroendocrine modulation of regulatory T lymphocyte system: in vivo and in vitro effects of the pineal immunomodulating hormone melatonin. In Vivo, 2010, 24(5), 787-789.
[PMID: 20952751]
[48]
Drum, C.L.; Tan, W.K.Y.; Chan, S.P.; Pakkiri, L.S.; Chong, J.P.C.; Liew, O.W.; Ng, T.P.; Ling, L.H.; Sim, D.; Leong, K.G.; Yeo, D.P.S.; Ong, H.Y.; Jaufeerally, F.; Wong, R.C.C.; Chai, P.; Low, A.F.; Davidsson, P.; Liljeblad, M.; Söderling, A.S.; Gan, L.M.; Bhat, R.V.; Purnamawati, K.; Lam, C.S.P.; Richards, A.M. Thymosin beta-4 is elevated in women with heart failure with preserved ejection fraction. J. Am. Heart Assoc., 2017, 6(6), e005586.
[http://dx.doi.org/10.1161/JAHA.117.005586 ] [PMID: 28611096]
[49]
Lagneux, C.; Joyeux, M.; Demenge, P.; Ribuot, C.; Godin-Ribuot, D. Protective effects of melatonin against ischemia reperfusion injury in the isolated rat heart. Life Sci., 2000, 66(6), 503-509.
[http://dx.doi.org/10.1016/S0024-3205(99)00620-7 ] [PMID: 10794067]
[50]
Sahna, E.; Acet, A.; Ozer, M.K.; Olmez, E. Myocardial ischemia-reperfusion in rats: reduction of infarct size by either supplemental physiological or pharmacological doses of melatonin. J. Pineal Res., 2002, 33(4), 234-238.
[http://dx.doi.org/10.1034/j.1600-079X.2002.02924.x ] [PMID: 12390506]
[51]
Petrosillo, G.; Colantuono, G.; Moro, N.; Ruggiero, F.M.; Tiravanti, E.; Di Venosa, N.; Fiore, T.; Paradies, G. Melatonin protects against heart ischemia reperfusion injury by inhibiting mitochondrial permeability transition pore opening. Am. J. Physiol. Heart Circ. Physiol., 2009, 297(4), H1487-H1493.
[http://dx.doi.org/10.1152/ajpheart.00163.2009 ] [PMID: 19684190]
[52]
Jia, P.; Liu, C.; Wu, N.; Jia, D.; Sun, Y. Agomelatine protects against myocardial ischemia reperfusion injury by inhibiting mitochondrial permeability transition pore opening. Am. J. Transl. Res., 2018, 10(5), 1310-1323.
[PMID: 29887947]
[53]
Odinokova, I.; Baburina, Y.; Kruglov, A.; Fadeeva, I.; Zvyagina, A.; Sotnikova, L.; Akatov, V.; Krestinina, O. Effect of melatonin on rat heart mitochondria in acute heart failure in aged rats. Int. J. Mol. Sci., 2018, 19(6), 1555.
[http://dx.doi.org/10.3390/ijms19061555 ] [PMID: 29882895]
[54]
Acikel, M.; Buyukokuroglu, M.E.; Aksoy, H.; Erdogan, F.; Erol, M.K. Protective effects of melatonin against myocardial injury induced by isoproterenol in rats. J. Pineal Res., 2003, 35(2), 75-79.
[http://dx.doi.org/10.1034/j.1600-079X.2003.00056.x ] [PMID: 12887648]
[55]
Mukherjee, D.; Ghosh, A.K.; Bandyopadhyay, A.; Basu, A.; Datta, S.; Pattari, S.K.; Reiter, R.J.; Bandyopadhyay, D. Melatonin protects against isoproterenol-induced alterations in cardiac mitochondrial energy-metabolizing enzymes, apoptotic proteins, and assists in complete recovery from myocardial injury in rats. J. Pineal Res., 2012, 53(2), 166-179.
[http://dx.doi.org/10.1111/j.1600-079X.2012.00984.x ] [PMID: 23050266]
[56]
Kalkan, F.; Parlakpinar, H.; Disli, O.M.; Tanriverdi, L.H.; Ozhan, O.; Polat, A.; Cetin, A.; Vardi, N.; Otlu, Y.O.; Acet, A. Protective and therapeutic effects of dexpanthenol on isoproterenol-induced cardiac damage in rats. J. Cell. Biochem., 2018, 119(9), 7479-7489.
[http://dx.doi.org/10.1002/jcb.27058 ] [PMID: 29775243]
[57]
Baykan, A.; Narin, N.; Narin, F.; Akgün, H.; Yavaşcan, S.; Saraymen, R. The protective effect of melatonin on nicotine-induced myocardial injury in newborn rats whose mothers received nicotine. Anadolu Kardiyol. Derg., 2008, 8(4), 243-248.
[PMID: 18676298]
[58]
Yildiz, A.; Vardi, N.; Karaaslan, M.G.; Ates, B.; Taslidere, E.; Esrefoglu, M. The protective effect of melatonin in lungs of newborn rats exposed to maternal nicotine. Biotech. Histochem., 2018, 93(6), 442-452.
[http://dx.doi.org/10.1080/10520295.2018.1453548 ] [PMID: 29701082]
[59]
Drobnik, J.; Karbownik-Lewińska, M.; Szczepanowska, A.; Słotwińska, D.; Olczak, S.; Jakubowski, L.; Dąbrowski, R. Regulatory influence of melatonin on collagen accumulation in the infarcted heart scar. J. Pineal Res., 2008, 45(3), 285-290.
[http://dx.doi.org/10.1111/j.1600-079X.2008.00588.x ] [PMID: 18384532]
[60]
Drobnik, J.; Olczak, S.; Owczarek, K.; Hrabec, Z.; Hrabec, E. Melatonin augments expression of the procollagen α1 (I) and α1 (III) genes in the infarcted heart scar of pinealectomized rats. Connect. Tissue Res., 2010, 51(6), 491-496.
[http://dx.doi.org/10.3109/03008201003686966 ] [PMID: 20388018]
[61]
Drobnik, J.; Slotwinska, D.; Olczak, S.; Tosik, D.; Pieniazek, A.; Matczak, K.; Koceva-Chyla, A.; Szczepanowska, A. Pharmacological doses of melatonin reduce the glycosaminoglycan level within the infarcted heart scar. J. Physiol. Pharmacol., 2011, 62(1), 29-35.
[PMID: 21451207]
[62]
Quan, Z.; Wang, Q-L.; Zhou, P.; Wang, G-D.; Tan, Y-Z.; Wang, H-J. Thymosin β4 promotes the survival and angiogenesis of transplanted endothelial progenitor cells in the infarcted myocardium. Int. J. Mol. Med., 2017, 39(6), 1347-1356.
[http://dx.doi.org/10.3892/ijmm.2017.2950 ] [PMID: 28440414]
[63]
Sewerynek, E. Melatonin and the cardiovascular system. Neuroendocrinol. Lett., 2002, 23(Suppl. 1), 79-83.
[PMID: 12019357]
[64]
Zhang, H.; Liu, D.; Wang, X.; Chen, X.; Long, Y.; Chai, W.; Zhou, X.; Rui, X.; Zhang, Q.; Wang, H.; Yang, Q. Melatonin improved rat cardiac mitochondria and survival rate in septic heart injury. J. Pineal Res., 2013, 55(1), 1-6.
[http://dx.doi.org/10.1111/jpi.12033 ] [PMID: 23330702]
[65]
Zhou, H.; Ma, Q.; Zhu, P.; Ren, J.; Reiter, R.J.; Chen, Y. Protective role of melatonin in cardiac ischemia-reperfusion injury: From pathogenesis to targeted therapy. J. Pineal Res., 2018, 64(3), e12471.
[http://dx.doi.org/10.1111/jpi.12471 ] [PMID: 29363153]
[66]
Petrosillo, G.; Moro, N.; Paradies, V.; Ruggiero, F.M.; Paradies, G. Increased susceptibility to Ca(2+)-induced permeability transition and to cytochrome c release in rat heart mitochondria with aging: effect of melatonin. J. Pineal Res., 2010, 48(4), 340-346.
[http://dx.doi.org/10.1111/j.1600-079X.2010.00758.x ] [PMID: 20345745]
[67]
Grossman, E.; Laudon, M.; Zisapel, N. Effect of melatonin on nocturnal blood pressure: meta-analysis of randomized controlled trials. Vasc. Health Risk Manag., 2011, 7, 577-584.
[http://dx.doi.org/10.2147/VHRM.S24603 ] [PMID: 21966222]
[68]
Baker, J.; Kimpinski, K. Role of melatonin in blood pressure regulation: An adjunct anti-hypertensive agent. Clin. Exp. Pharmacol. Physiol., 2018, 45(8), 755-766.
[http://dx.doi.org/10.1111/1440-1681.12942 ] [PMID: 29603319]
[69]
Molinero, P.; Soutto, M.; Benot, S.; Hmadcha, A.; Guerrero, J.M. Melatonin is responsible for the nocturnal increase observed in serum and thymus of thymosin α1 and thymulin concentrations: observations in rats and humans. J. Neuroimmunol., 2000, 103(2), 180-188.
[http://dx.doi.org/10.1016/S0165-5728(99)00237-4 ] [PMID: 10696913]
[70]
Navarro-Alarcon, M.; Ruiz-Ojeda, F.J.; Blanca-Herrera, R.M.; Agil, A. Antioxidant activity of melatonin in diabetes in relation to the regulation and levels of plasma Cu, Zn, Fe, Mn, and Se in Zucker diabetic fatty rats. Nutrition, 2013, 29(5), 785-789.
[http://dx.doi.org/10.1016/j.nut.2012.11.005 ] [PMID: 23352467]
[71]
Tarantino, G.; Porcu, C.; Arciello, M.; Andreozzi, P.; Balsano, C. Prediction of carotid intima-media thickness in obese patients with low prevalence of comorbidities by serum copper bioavailability. J. Gastroenterol. Hepatol., 2018, 33(8), 1511-1517.
[http://dx.doi.org/10.1111/jgh.14104 ] [PMID: 29405466]
[72]
Young, J.D.; Lawrence, A.J.; MacLean, A.G.; Leung, B.P.; McInnes, I.B.; Canas, B.; Pappin, D.J.; Stevenson, R.D. Thymosin β 4 sulfoxide is an anti-inflammatory agent generated by monocytes in the presence of glucocorticoids. Nat. Med., 1999, 5(12), 1424-1427.
[http://dx.doi.org/10.1038/71002 ] [PMID: 10581087]
[73]
Nakamura, M.; Kawahara, M.; Nakata, K.; Nishida, T. Restoration of corneal epithelial barrier function and wound healing by substance P and IGF-1 in rats with capsaicin-induced neurotrophic keratopathy. Invest. Ophthalmol. Vis. Sci., 2003, 44(7), 2937-2940.
[http://dx.doi.org/10.1167/iovs.02-0868 ] [PMID: 12824234]
[74]
Wang, H.; Ji, B.; Liu, X.S.; van Oers, R.F.; Guo, X.E.; Huang, Y.; Hwang, K-C. Osteocyte-viability-based simulations of trabecular bone loss and recovery in disuse and reloading. Biomech. Model. Mechanobiol., 2014, 13(1), 153-166.
[http://dx.doi.org/10.1007/s10237-013-0492-1 ] [PMID: 23584331]
[75]
Burbach, G.J.; Kim, K.H.; Zivony, A.S.; Kim, A.; Aranda, J.; Wright, S.; Naik, S.M.; Caughman, S.W.; Ansel, J.C.; Armstrong, C.A. The neurosensory tachykinins substance P and neurokinin A directly induce keratinocyte nerve growth factor. J. Invest. Dermatol., 2001, 117(5), 1075-1082.
[http://dx.doi.org/10.1046/j.0022-202x.2001.01498.x ] [PMID: 11710915]
[76]
Rook, J.M.; McCarson, K.E. Delay of cutaneous wound closure by morphine via local blockade of peripheral tachykinin release. Biochem. Pharmacol., 2007, 74(5), 752-757.
[http://dx.doi.org/10.1016/j.bcp.2007.06.005 ] [PMID: 17632084]
[77]
Zhu, F.; Liu, D.; Zhang, H.; Xu, J.; Peng, Y.; Zhong, Q.; Li, Y. Effect of substance P combined with epidermal stem cells on wound healing and nerve regeneration in rats with diabetes mellitus. Zhonghua shao shang za zhi= Zhonghua shaoshang zazhi= Chinese journal of burns., 2012, 28(1), 25-31.
[http://dx.doi.org/10.3760/cma.j.issn.1009-2587.2012.01. 007] [PMID: 22490536]
[78]
Suzuki, A.; Uemura, T.; Nakamura, H. [Control of bone remodeling by nervous system. Neural involvement in fracture healing and bone regeneration] Clin. Calcium, 2010, 20(12), 1820-1827.
[PMID: 21123934]
[79]
Zhou, Y.; Zhang, M.; Sun, G-Y.; Liu, Y-P.; Ran, W-Z.; Peng, L.; Guan, C-X. Calcitonin gene-related peptide promotes the wound healing of human bronchial epithelial cells via PKC and MAPK pathways. Regul. Pept., 2013, 184, 22-29.
[http://dx.doi.org/10.1016/j.regpep.2013.03.020 ] [PMID: 23501044]
[80]
Evangelista, S. Role of calcitonin gene-related Peptide in gastric mucosal defence and healing. Curr. Pharm. Des., 2009, 15(30), 3571-3576.
[http://dx.doi.org/10.2174/138161209789207024 ] [PMID: 19860701]
[81]
Felderbauer, P.; Bulut, K.; Hoeck, K.; Deters, S.; Schmidt, W.E.; Hoffmann, P. Substance P induces intestinal wound healing via fibroblasts--evidence for a TGF-β-dependent effect. Int. J. Colorectal Dis., 2007, 22(12), 1475-1480.
[http://dx.doi.org/10.1007/s00384-007-0321-z ] [PMID: 17520266]
[82]
Xinan, L.; Suguang, L.; Liangchao, Z.; Lei, C. Change in substance P in a firearm wound and its significance. Peptides, 1998, 19(7), 1209-1212.
[http://dx.doi.org/10.1016/S0196-9781(98)00068-0 ] [PMID: 9786170]
[83]
Sharma, S.; Gupta, R.; Nautiyal, A.; Sindhwani, G. Effects of ergoreflex on respiration and other efferent effects in adult male patients with chronic obstructive pulmonary disease. Indian J. Physiol. Pharmacol., 2012, 56(3), 201-212.
[PMID: 23734433]
[84]
Bellayr, I.; Holden, K.; Mu, X.; Pan, H.; Li, Y. Matrix metalloproteinase inhibition negatively affects muscle stem cell behavior. Int. J. Clin. Exp. Pathol., 2013, 6(2), 124-141.
[PMID: 23329998]
[85]
Fujimaki, S.; Machida, M.; Hidaka, R.; Asashima, M.; Takemasa, T.; Kuwabara, T. Intrinsic ability of adult stem cell in skeletal muscle: an effective and replenishable resource to the establishment of pluripotent stem cells. Stem Cells Int., 2013, 2013, 420164.
[http://dx.doi.org/10.1155/2013/420164 ] [PMID: 23818907]
[86]
André, L.M.; Ausems, C.R.M.; Wansink, D.G.; Wieringa, B. Abnormalities in skeletal muscle myogenesis, growth, and regeneration in myotonic dystrophy. Front. Neurol., 2018, 9, 368.
[http://dx.doi.org/10.3389/fneur.2018.00368 ] [PMID: 29892259]
[87]
Pallafacchina, G.; Blaauw, B.; Schiaffino, S. Role of satellite cells in muscle growth and maintenance of muscle mass. Nutr. Metab. Cardiovasc. Dis., 2013, 23(Suppl. 1), S12-S18.
[http://dx.doi.org/10.1016/j.numecd.2012.02.002 ] [PMID: 22621743]
[88]
Schiaffino, S.; Dyar, K.A.; Ciciliot, S.; Blaauw, B.; Sandri, M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J., 2013, 280(17), 4294-4314.
[http://dx.doi.org/10.1111/febs.12253 ] [PMID: 23517348]
[89]
Tarnopolsky, M.A. Mitochondrial DNA shifting in older adults following resistance exercise training. Appl. Physiol. Nutr. Metab., 2009, 34(3), 348-354.
[http://dx.doi.org/10.1139/H09-022 ] [PMID: 19448697]
[90]
Jain, M.; LoGerfo, F.W.; Guthrie, P.; Pradhan, L. Effect of hyperglycemia and neuropeptides on interleukin-8 expression and angiogenesis in dermal microvascular endo-thelial cells. J. Vasc. Surg., 2011, 53(6), 1654-1660.
[http://dx.doi.org/10.1016/j.jvs.2011.02.019]]
[91]
Mapp, P.I.; McWilliams, D.F.; Turley, M.J.; Hargin, E.; Walsh, D.A. A role for the sensory neuropeptide calcitonin gene-related peptide in endothelial cell proliferation in vivo. Br. J. Pharmacol., 2012, 166(4), 1261-1271.
[http://dx.doi.org/10.1111/j.1476-5381.2012.01848.x ] [PMID: 22233274]
[92]
Koon, H-W.; Zhao, D.; Xu, H.; Bowe, C.; Moss, A.; Moyer, M.P.; Pothoulakis, C. Substance P-mediated expression of the pro-angiogenic factor CCN1 modulates the course of colitis. Am. J. Pathol., 2008, 173(2), 400-410.
[http://dx.doi.org/10.2353/ajpath.2008.080222 ] [PMID: 18599605]
[93]
Toda, M.; Suzuki, T.; Hosono, K.; Kurihara, Y.; Kurihara, H.; Hayashi, I.; Kitasato, H.; Hoka, S.; Majima, M. Roles of calcitonin gene-related peptide in facilitation of wound healing and angiogenesis. Biomed. Pharmacother., 2008, 62(6), 352-359.
[http://dx.doi.org/10.1016/j.biopha.2008.02.003 ] [PMID: 18430544]
[94]
Tuhy, Ł.; Dmytryk, A.; Samoraj, M.; Chojnacka, K. Trace Elements in Animal Nutrition. Recent Advances in Trace Elements; Chojnacka, K; Saeid, A., Ed.; Wiley, 2018, pp. 319-337.
[http://dx.doi.org/10.1002/9781119133780.ch16]
[95]
Correll, C.C.; Phelps, P.T.; Anthes, J.C.; Umland, S.; Greenfeder, S. Cloning and pharmacological characterization of mouse TRPV1. Neurosci. Lett., 2004, 370(1), 55-60.
[http://dx.doi.org/10.1016/j.neulet.2004.07.058 ] [PMID: 15489017]
[96]
Geppetti, P.; Trevisani, M. Activation and sensitisation of the vanilloid receptor: role in gastrointestinal inflammation and function. Br. J. Pharmacol., 2004, 141(8), 1313-1320.
[http://dx.doi.org/10.1038/sj.bjp.0705768 ] [PMID: 15051629]
[97]
Assas, B.M.; Pennock, J.I.; Miyan, J.A. Calcitonin gene-related peptide is a key neurotransmitter in the neuro-immune axis. Front. Neurosci., 2014, 8, 23.
[http://dx.doi.org/10.3389/fnins.2014.00023 ] [PMID: 24592205]
[98]
Smith, D.R.; Kahng, M.W.; Quintanilla-Vega, B.; Fowler, B.A. High-affinity renal lead-binding proteins in environmentally-exposed humans. Chem. Biol. Interact., 1998, 115(1), 39-52.
[http://dx.doi.org/10.1016/S0009-2797(98)00060-X ] [PMID: 9817074]
[99]
Chaumont, A.; Nickmilder, M.; Dumont, X.; Lundh, T.; Skerfving, S.; Bernard, A. Associations between proteins and heavy metals in urine at low environmental exposures: evidence of reverse causality. Toxicol. Lett., 2012, 210(3), 345-352.
[http://dx.doi.org/10.1016/j.toxlet.2012.02.005 ] [PMID: 22353377]
[100]
Askarian, M.; Mansour Ghanaie, R.; Karimi, A.; Habibzadeh, F. Infectious diseases in Iran: a bird’s eye view. Clin. Microbiol. Infect., 2012, 18(11), 1081-1088.
[http://dx.doi.org/10.1111/1469-0691.12021 ] [PMID: 23033964]
[101]
Needleman, H.; Riess, J.; Tobin, M.; Biesecker, G.; Greenhouse, J. Bone lead levels and delinquent behavior. JAMA, 1996, 275, 363-369.
[http://dx.doi.org/10.1001/jama.1996.03530290033034 ]
[102]
Needleman, H.L.; McFarland, C.; Ness, R.B.; Fienberg, S.E.; Tobin, M.J. Bone lead levels in adjudicated delinquents. A case control study. Neurotoxicol. Teratol., 2002, 24(6), 711-717.
[http://dx.doi.org/10.1016/S0892-0362(02)00269-6 ] [PMID: 12460653]
[103]
Nicolescu, R.; Petcu, C.; Cordeanu, A.; Fabritius, K.; Schlumpf, M.; Krebs, R.; Krämer, U.; Winneke, G. Environmental exposure to lead, but not other neurotoxic metals, relates to core elements of ADHD in Romanian children: performance and questionnaire data. Environ. Res., 2010, 110(5), 476-483.
[http://dx.doi.org/10.1016/j.envres.2010.04.002 ] [PMID: 20434143]
[104]
Yousef, S.; Adem, A.; Zoubeidi, T.; Kosanovic, M.; Mabrouk, A.A.; Eapen, V. Attention deficit hyperactivity disorder and environmental toxic metal exposure in the United Arab Emirates. J. Trop. Pediatr., 2011, 57(6), 457-460.
[http://dx.doi.org/10.1093/tropej/fmq121 ] [PMID: 21300623]
[105]
Bouchard, M.F.; Bellinger, D.C.; Weuve, J.; Matthews-Bellinger, J.; Gilman, S.E.; Wright, R.O.; Schwartz, J.; Weisskopf, M.G. Blood lead levels and major depressive disorder, panic disorder, and generalized anxiety disorder in US young adults. Arch. Gen. Psychiatry, 2009, 66(12), 1313-1319.
[http://dx.doi.org/10.1001/archgenpsychiatry.2009.164 ] [PMID: 19996036]
[106]
Bock-Marquette, I.; Saxena, A.; White, M.D.; Dimaio, J.M.; Srivastava, D. Thymosin β4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature, 2004, 432(7016), 466-472.
[http://dx.doi.org/10.1038/nature03000 ] [PMID: 15565145]
[107]
Srivastava, D.; Saxena, A.; Michael Dimaio, J.; Bock-Marquette, I. Thymosin β4 is cardioprotective after myocardial infarction. Ann. N. Y. Acad. Sci., 2007, 1112(1), 161-170.
[http://dx.doi.org/10.1196/annals.1415.048 ] [PMID: 17600280]
[108]
Zhao, Y.; Song, J.; Bi, X.; Gao, J.; Shen, Z.; Zhu, J.; Fu, G. Thymosin β4 promotes endothelial progenitor cell angiogenesis via a vascular endothelial growth factordependent mechanism. Mol. Med. Rep., 2018, 18(2), 2314-2320.
[http://dx.doi.org/10.3892/mmr.2018.9199 ] [PMID: 29956769]
[109]
Morita, T.; Hayashi, K. Tumor progression is mediated by thymosin-ß4 through a TGFß/MRTF signaling axis. Mol. Cancer Res., 2018, 16(5), 880-893.
[http://dx.doi.org/10.1158/1541-7786.MCR-17-0715 ] [PMID: 29330296]
[110]
Morita, T.; Hayashi, K. G-actin sequestering protein thymosin-β4 regulates the activity of myocardin-related transcription factor. Biochem. Biophys. Res. Commun., 2013, 437(3), 331-335.
[http://dx.doi.org/10.1016/j.bbrc.2013.06.069 ] [PMID: 23811404]
[111]
Qian, L.; Huang, Y.; Spencer, C.I.; Foley, A.; Vedantham, V.; Liu, L.; Conway, S.J.; Fu, J.D.; Srivastava, D. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature, 2012, 485(7400), 593-598.
[http://dx.doi.org/10.1038/nature11044 ] [PMID: 22522929]
[112]
Srivastava, D.; Ieda, M.; Fu, J.; Qian, L. Cardiac repair with thymosin β4 and cardiac reprogramming factors. Ann. N. Y. Acad. Sci., 2012, 1270(1), 66-72.
[http://dx.doi.org/10.1111/j.1749-6632.2012.06696.x ] [PMID: 23050819]
[113]
Melov, S.; Tarnopolsky, M.A.; Beckman, K.; Felkey, K.; Hubbard, A. Resistance exercise reverses aging in human skeletal muscle. PLoS One, 2007, 2(5), e465.
[http://dx.doi.org/10.1371/journal.pone.0000465] [PMID: 17520024]
[114]
Hara, T. Thymosins and Muscle Regeneration. In: Vitamins and Hormones; Elsevier, 2011; Vol. 87, pp. 277-290.
[http://dx.doi.org/10.1016/B978-0-12-386015-6.00032-9.]
[115]
Matsuo, K.; Akasaki, Y.; Adachi, K.; Zhang, M.; Ishikawa, A.; Jimi, E.; Nishihara, T.; Hosokawa, R. Promoting effects of thymosin β4 on granulation tissue and new bone formation after tooth extraction in rats. Oral Surg. Oral Med. Oral Pathol. Oral Radiol., 2012, 114(1), 17-26.
[http://dx.doi.org/10.1016/j.tripleo.2011.05.025 ] [PMID: 22732845]
[116]
Adachi, K.; Matsuo, K.; Akasaki, Y.; Kanao, M.; Maeda, T.; Ishikawa, A.; Hosokawa, R. Effects of thymosin β4 on the bone formation of calvarial defects in rats. J. Prosthodont. Res., 2013, 57(3), 162-168.
[http://dx.doi.org/10.1016/j.jpor.2013.01.008 ] [PMID: 23490448]
[117]
Treadwell, T.; Kleinman, H.K.; Crockford, D.; Hardy, M.A.; Guarnera, G.T.; Goldstein, A.L. The regenerative peptide thymosin β4 accelerates the rate of dermal healing in preclinical animal models and in patients. Ann. N. Y. Acad. Sci., 2012, 1270(1), 37-44.
[http://dx.doi.org/10.1111/j.1749-6632.2012.06717.x ] [PMID: 23050815]
[118]
Zomer, H.D.; Trentin, A.G. Skin wound healing in humans and mice: Challenges in translational research. J. Dermatol. Sci., 2018, 90(1), 3-12.
[http://dx.doi.org/10.1016/j.jdermsci.2017.12.009 ] [PMID: 29289417]
[119]
Zuo, Y.; Chun, B.; Potthoff, S.A.; Kazi, N.; Brolin, T.J.; Orhan, D.; Yang, H-C.; Ma, L-J.; Kon, V.; Myöhänen, T.; Rhaleb, N.E.; Carretero, O.A.; Fogo, A.B. Thymosin β4 and its degradation product, Ac-SDKP, are novel reparative factors in renal fibrosis. Kidney Int., 2013, 84(6), 1166-1175.
[http://dx.doi.org/10.1038/ki.2013.209 ] [PMID: 23739235]
[120]
Tokura, Y.; Nakayama, Y.; Fukada, S.; Nara, N.; Yamamoto, H.; Matsuda, R.; Hara, T. Muscle injury-induced thymosin β4 acts as a chemoattractant for myoblasts. J. Biochem., 2011, 149(1), 43-48.
[http://dx.doi.org/10.1093/jb/mvq115 ] [PMID: 20880960 ]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy