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Proteomic profile associated with cell death induced by androgens in Taenia crassiceps cysticerci: proposed interactome

Published online by Cambridge University Press:  28 August 2018

J.R. Ambrosio ,
M.I. Palacios-Arreola ,
D.G. Ríos-Valencia ,
O. Reynoso-Ducoing ,
K.E. Nava-Castro ,
P. Ostoa-Saloma  and
J. Morales-Montor Open the ORCID record for J. Morales-Montor [Opens in a new window]
J.R. Ambrosio
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de Mexico (UNAM), Edificio A, 2do piso, Ciudad Universitaria, Ciudad de México, 04510, Mexico
M.I. Palacios-Arreola
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, AP 70228, Ciudad de México, 04510, Mexico Laboratorio de Genotoxicología y Mutagénesis Ambiental, Departamento de Ciencias Ambientales, Centro de Ciencias de la Atmósfera, Universidad Nacional Autónoma de México. Ciudad de México, 04510, Mexico
D.G. Ríos-Valencia
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de Mexico (UNAM), Edificio A, 2do piso, Ciudad Universitaria, Ciudad de México, 04510, Mexico
O. Reynoso-Ducoing
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de Mexico (UNAM), Edificio A, 2do piso, Ciudad Universitaria, Ciudad de México, 04510, Mexico
K.E. Nava-Castro
Affiliation:
Laboratorio de Genotoxicología y Mutagénesis Ambiental, Departamento de Ciencias Ambientales, Centro de Ciencias de la Atmósfera, Universidad Nacional Autónoma de México. Ciudad de México, 04510, Mexico
P. Ostoa-Saloma
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, AP 70228, Ciudad de México, 04510, Mexico
J. Morales-Montor*
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, AP 70228, Ciudad de México, 04510, Mexico
*
Author for correspondence: J. Morales-Montor E-mail: [email protected][email protected]
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Abstract

Androgens have been shown to exert a cysticidal effect upon Taenia crassiceps, an experimental model of cysticercosis. To further inquire into this matter, the Taenia crassiceps model was used to evaluate the expression of several proteins after testosterone (T4) and dihydrotestosterone (DHT) in vitro treatment. Under 2-D proteomic maps, parasite extracts were resolved into approximately 130 proteins distributed in a molecular weight range of 10–250 kDa and isoelectrical point range of 3–10. The resultant proteomic pattern was analysed, and significant changes were observed in response to T4 and DHT. Based on our experience with electrophoretic patterns and proteomic maps of cytoskeletal proteins, alteration in the expression of isoforms of actin, tubulin and paramyosin and of other proteins was assessed. Considering that androgens may exert their biological activity in taeniids through the non-specific progesterone receptor membrane component (PGRMC), we harnessed bioinformatics to propose the identity of androgen-regulated proteins and establish their hypothetical physiological role in the parasites. These analyses yield a possible explanation of how androgens exert their cysticidal effects through changes in the expression of proteins involved in cytoskeletal rearrangement, dynamic vesicular traffic and transduction of intracellular signals.

Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 5 , September 2019 , pp. 539 - 547
Copyright
Copyright © Cambridge University Press 2018 

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References

Aguilar-Díaz, H et al. (2018) A novel progesterone receptor membrane component (PGRMC) in the human and swine parasite Taenia solium: implications to the host–parasite relationship. Parasites & Vectors 11, 161.Google Scholar
Almeida, CR et al. (2009) Transcriptome analysis of Taenia solium cysticerci using Open Reading Frame ESTs (ORESTES). Parasites & Vectors 2, 35.Google Scholar
Alvarez, LI, Mottier, ML and Lanusse, CE (2007) Drug transfer into target helminth parasites. Trends in Parasitology 23, 97–104.Google Scholar
Ambrosio, JR et al. (2003) Actin expression in Taenia solium cysticerci (cestoda): Tisular distribution and detection of isoforms. Cell Biology International 27, 727–733.Google Scholar
Ambrosio, JR et al. (2014) Oestradiol and progesterone differentially alter cytoskeletal protein expression and flame cell morphology in Taenia crassiceps. International Journal for Parasitology 44, 687–696.Google Scholar
Ambrosio, JR et al. (2015) Androgens exert a cysticidal effect upon Taenia crassiceps by disrupting flame cell morphology and function. PLoS ONE 10, e0127928.Google Scholar
Benboudjema, L et al. (2003) Association of the herpes simplex virus type 1 Us11 gene product with the cellular kinesin light-chain-related protein PAT1 results in the redistribution of both polypeptides. Journal of Virology 77, 9192–9203.Google Scholar
Bhai, I and Pandey, AK (1982) Gonadal hormones in experimental Ancylostoma caninum infections in male Swiss albino mice. International Journal for Parasitology 12, 589–591.Google Scholar
Colello, D et al. (2010) Androgen and Src signaling regulate centrosome activity. Journal of Cell Science 123(Pt 12), 2094–2102.Google Scholar
Corbett, AH and Silver, PA (1997) Nucleocytoplasmic transport of macromolecules. Microbiology and Molecular Biology Reviews 61, 193–211.Google Scholar
Escobedo, G et al. (2004) Molecular mechanisms involved in the differential effects of sex steroids on the reproduction and infectivity of Taenia crassiceps. Journal of Parasitology 90, 1235–1244.Google Scholar
Escobedo, G et al. (2005) Parasite regulation by host hormones: an old mechanism of host exploitation? Trends in Parasitology 21, 588–593.Google Scholar
Escobedo, G et al. (2010a) Progesterone induces scolex evagination of the human parasite Taenia solium: evolutionary implications to the host–parasite relationship. Journal of Biomedicine and Biotechnology 2010, 591079.Google Scholar
Escobedo, G et al. (2010b) A new MAP kinase protein involved in estradiol-stimulated reproduction of the helminth parasite Taenia crassiceps. Journal of Biomedicine and Biotechnology 2010, 747121.Google Scholar
Escobedo, G et al. (2011) Progesterone induces mucosal immunity in a rodent model of human taeniosis by Taenia solium. International Journal of Biological Sciences 7, 1443–1456.Google Scholar
García-Montoya, GM et al. (2015) Transcriptome profiling of the cysticercus stage of the laboratory model Taenia crassiceps, strain ORF. Acta Tropica 154, 50–62.Google Scholar
Gerke, V and Moss, SE (2002) Annexins: from structure to function. Physiological Reviews 82, 331–371.Google Scholar
Glover, JNM and Harrison, SC (1995) Crystal structure of the heterodimeric bZIP transcription factor c-Fos–c-Jun bound to DNA. Nature 373, 257–261.Google Scholar
Gu, S et al. (2009) Functional membrane androgen receptors in colon tumors trigger pro-apoptotic responses in vitro and reduce drastically tumor incidence in vivo. Molecular Cancer 8, 114.Google Scholar
Hernández-Bello, R et al. (2011) Sex steroids effects on the molting process of the helminth human parasite Trichinella spiralis. Journal of Biomedicine and Biotechnology 2011, 625380.Google Scholar
Hlavaty, J et al. (2016) Expression of progesterone receptor membrane component 1 (PGRMC1), progestin and AdipoQ receptor 7 (PAQPR7), and plasminogen activator inhibitor 1 RNA-binding protein (PAIRBP1) in glioma spheroids in vitro. Biomed Research International 2016, 8065830.Google Scholar
Hu, W et al. (2003) Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nature Genetics 35, 139–147.Google Scholar
Huerta, L et al. (1992) Immunological mediation of gonadal effects on experimental murine cysticercosis caused by Taenia crassiceps metacestodes. Journal of Parasitology 78, 471–476.Google Scholar
Ibarra-Coronado, EG et al. (2011) A helminth cestode parasite express an estrogen-binding protein resembling a classic nuclear estrogen receptor. Steroids 76, 1149–1159.Google Scholar
Johnson, GL and Lapadat, R (2002) Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298, 1911–1912.Google Scholar
Kipp, JL and Ramirez, VD (2003) Estradiol and testosterone have opposite effects on microtubule polymerization. Neuroendocrinology 77, 258–272.Google Scholar
Lange, CA (2004) Making sense of cross-talk between steroid hormone receptors and intracellular signaling pathways: who will have the last word? Molecular Endocrinology 18, 269–278.Google Scholar
Larralde, C et al. (1990) Immunodiagnosis of human cysticercosis in cerebrospinal fluid. Antigens from murine Taenia crassiceps cysticerci effectively substitute those from porcine Taenia solium. Archives of Pathology & Laboratory Medicine 114, 926–928.Google Scholar
Larralde, C et al. (1995) Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. Journal of Steroid Biochemistry and Molecular Biology 52, 575–580.Google Scholar
Melendez, J, Grogg, M and Zheng, Y (2011) Signaling role of Cdc42 in regulating mammalian physiology. Journal of Biological Chemistry 286, 2375–2381.Google Scholar
Migliaccio, A et al. (1998) Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO Journal 17, 2008–2018.Google Scholar
Mistry, SJ and Oh, WK (2013) New paradigms in microtubule-mediated endocrine signaling in prostate cancer. Molecular Cancer Therapeutics 12, 555–566.Google Scholar
Morales-Montor, J et al. (2002a) Taenia crassiceps: androgen reconstitution of the host leads to protection during cysticercosis. Experimental Parasitology 100, 209–216.Google Scholar
Morales-Montor, J et al. (2002b) Inhibition of p-450 aromatase prevents feminisation and induces protection during cysticercosis. International Journal of Parasitology 32, 1379–1387.Google Scholar
Papadopoulou, N et al. (2009) Membrane androgen receptor activation in prostate and breast tumor cells: molecular signaling and clinical impact. IUBMB Life 61, 56–61.Google Scholar
Papakonstanti, EA et al. (2003) A rapid, nongenomic signaling pathway regulates the actin reorganization induced by activation of membrane testosterone receptors. Molecular Endocrinology 17, 870–881.Google Scholar
Reynoso-Ducoing, O et al. (2014) Analysis of the expression of cytoskeletal proteins of Taenia crassiceps ORF strain cysticerci (Cestoda). Parasitology Research 113, 1955–1969.Google Scholar
Smith, JK, Esch, GW and Kuhn, RE (1972) Growth and development of larval Taenia crassiceps (cestoda). I. Aneuplody in the anomalous ORF strain. International Journal of Parasitology 2, 261–263.Google Scholar
Stournaras, C et al. (2014) The actin cytoskeleton in rapid steroid hormone actions. Cytoskeleton 71, 285–293.Google Scholar
Tsai, IJ et al. (2013) The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57–63.Google Scholar
Vale, RD (2003) The molecular motor toolbox for intracellular transport. Cell 112, 467–480.Google Scholar
Vargas-Villavicencio, JA et al. (2005) Regulation of the immune response to cestode infection by progesterone is due to its metabolism to estradiol. Microbes and Infection 7, 485–493.Google Scholar
Vargas-Villavicencio, JA, Larralde, C and Morales-Montor, J (2006) Gonadectomy and progesterone treatment induce protection in murine cysticercosis. Parasite Immunology 28, 667–674.Google Scholar
Virginio, VG et al. (2012) Excretory/secretory products from in vitro-cultured Echinococcus granulosus protoscoleces. Molecular and Biochemical Parasitology 183, 15–22.Google Scholar
Walenta, JH et al. (2001) The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. Journal of Cell Biology 152, 923–934.Google Scholar
Wu, X et al. (2012) Detailed transcriptome description of the neglected cestode Taenia multiceps. PLoS ONE 7(9), e45830.Google Scholar
Yamaji, S et al. (2001) A novel integrin-linked kinase-binding protein, affixin, is involved in the early stage of cell–substrate interaction. Journal of Cell Biology 153, 125–164.Google Scholar
Yan, S et al. (2015) Atomic-resolution structure of the CAP-Gly domain of dynactin on polymeric microtubules determined by magic angle spinning NMR spectroscopy. Proceedings of the National Academy of Sciences 112, 14611–14616.Google Scholar
Yong, WK, Heath, DD and Van Knapen, F (1984) Comparison of cestode antigens in an enzyme-linked immunosorbent assay for the diagnosis of Echinococcus granulosus, Taenia hydatigena and T. ovis infections in sheep. Research Veterinary Science 36, 24–31.Google Scholar