Roles of microRNAs and Long Non-Coding RNAs Encoded by Parasitic Helminths in Human Carcinogenesis
<p>Helminths may promote tumorigenesis through different processes such as chronic inflammation; the polarization of immune cells such as macrophages and T cells; or by inducing persistent injury in the tissues, which can lead to undesirable effects such as fibrosis. miRNAs expressed and secreted by helminths involved in human cancer can modulate these processes. Some helminth miRNAs have shown direct antitumoral activity. miRNAs from parasites could be useful in therapy and diagnostics; for example, an miRNA of <span class="html-italic">S. haematobium</span> (Sha-mir-71a) is abundant in the urine of patients with bladder cancer associated with infection. Created using BioRender.com.</p> "> Figure 2
<p>Eggs of <span class="html-italic">S. Japonicum</span> can release extracellular vesicles, which transport different miRNA cargo that can be internalized by host cells as liver stellate cells and exert distinct effects. These miRNAs can repress the genic expression of host-cell molecular targets, promoting the activation of liver stellate cells. This has been associated with the generation of liver fibrosis. In contrast, Sja-mir-71a can inhibit the activation of stellate cells and prevent fibrosis. Additionally, Sja-mir-71a induces a reduction in Th1, Th2, and Th17 cells in the liver and spleen, having immunomodulatory functions that possibly influence the characteristics of the microenvironment in host tissues. Created using <a href="http://BioRender.com" target="_blank">BioRender.com</a>.</p> "> Figure 3
<p><span class="html-italic">S. japonicum</span> worms can release extracellular vesicles that transport miRNA cargo, such as Sja-mir-125b and Sja-bantam. These miRNAs are internalized by host macrophages, bind molecular targets, and induce a proinflammatory phenotype. Moreover, these miRNAs secreted by the worms promote the proliferation of macrophages. Created using <a href="http://BioRender.com" target="_blank">BioRender.com</a>.</p> "> Figure 4
<p><span class="html-italic">C. sinensis</span> worms can release extracellular vesicles with miRNA cargo such as Csi-let-7a-5p. This miRNA is delivered to host macrophages, binds molecular targets inhibiting genic expression, and promotes polarization of these immune cells. Csi-let-7a-5p packaged in extracellular vesicles supports the accumulation of M1-like macrophages in the liver, which can lead to a proinflammatory microenvironment that has been connected to damage and proliferation of biliary cells. Created using <a href="http://BioRender.com" target="_blank">BioRender.com</a>.</p> ">
Abstract
:1. Introduction
2. microRNAs (miRNAs)
3. Long Non-Coding RNAs (lncRNAs)
4. Helminths Involved in Cancer
4.1. Schistosoma Haematobium and Schistosoma Japonicum
4.2. Clonorchis Sinensis
4.3. Opisthorchis Viverrini
5. miRNAs of Schistosoma haematobium
Sha-miR-71a
6. LncRNAs of Schistosoma haematobium
7. miRNAs of Schistosoma japonicum
7.1. miRNAs in Development and Sexual Maturation
7.2. miRNAs and Liver Fibrosis: Sja-mir-1, Sja-mir-2162, and Sja-mir-71a
7.3. miRNAs and Immunomodulation: Sja-mir-125b, Sja-bantam, and Sja-mir-71a
7.4. Antitumoral miRNAs: Sja-mir-61, Sja-mir-7-5p, Sja-mir-71a, and Sja-mir-3096
7.5. Circulating miRNAs in Host Serum/Plasma
8. LncRNAs of Schistosoma japonicum
9. miRNAs of Clonorchis sinensis
Csi-let-7a-5p
10. miRNAs and lncRNAs of Opisthorchis viverrini
11. Conclusions and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Buccitelli, C.; Selbach, M. mRNAs, Proteins and the Emerging Principles of Gene Expression Control. Nat. Rev. Genet. 2020, 21, 630–644. [Google Scholar] [CrossRef] [PubMed]
- Karimi, P.; Bakhtiarizadeh, M.R.; Salehi, A.; Izadnia, H.R. Transcriptome Analysis Reveals the Potential Roles of Long Non-Coding RNAs in Feed Efficiency of Chicken. Sci. Rep. 2022, 12, 2558. [Google Scholar] [CrossRef] [PubMed]
- Xie, L.; Zhang, Q.; Mao, J.; Zhang, J.; Li, L. The Roles of LncRNA in Myocardial Infarction: Molecular Mechanisms, Diagnosis Biomarkers, and Therapeutic Perspectives. Front. Cell Dev. Biol. 2021, 9, 680713. [Google Scholar] [CrossRef]
- Zhang, P.; Wu, W.; Chen, Q.; Chen, M. Non-Coding RNAs and Their Integrated Networks. J. Integr. Bioinform. 2019, 16, 20190027. [Google Scholar] [CrossRef]
- Chowdhary, A.; Satagopam, V.; Schneider, R. Long Non-Coding RNAs: Mechanisms, Experimental, and Computational Approaches in Identification, Characterization, and Their Biomarker Potential in Cancer. Front. Genet. 2021, 12, 649619. [Google Scholar] [CrossRef]
- Sharma, Y.; Sharma, A.; Singh, K.; Upadhyay, S.K. Long Non-Coding RNAs as Emerging Regulators of Pathogen Response in Plants. NonCoding RNA 2022, 8, 4. [Google Scholar] [CrossRef]
- Wu, X.; Pan, Y.; Fang, Y.; Zhang, J.; Xie, M.; Yang, F.; Yu, T.; Ma, P.; Li, W.; Shu, Y. The Biogenesis and Functions of PiRNAs in Human Diseases. Mol. Ther. Nucleic Acids 2020, 21, 108–120. [Google Scholar] [CrossRef]
- Patop, I.L.; Wüst, S.; Kadener, S. Past, Present, and Future of Circ RNAs. EMBO J. 2019, 38, e100836. [Google Scholar] [CrossRef]
- Lin, L.; Li, Z.; Yan, L.; Liu, Y.; Yang, H.; Li, H. Global, Regional, and National Cancer Incidence and Death for 29 Cancer Groups in 2019 and Trends Analysis of the Global Cancer Burden, 1990–2019. J. Hematol. Oncol. 2021, 14, 197. [Google Scholar] [CrossRef]
- Hanahan, D. Hallmarks of Cancer: New Dimensions. Cancer Discov. 2022, 12, 31–46. [Google Scholar] [CrossRef]
- Orendain-Jaime, E.N.; Serafín-Higuera, N.; Leija-Montoya, A.G.; Martínez-Coronilla, G.; Moreno-Trujillo, M.; Sánchez-Muñoz, F.; Ruiz-Hernández, A.; González-Ramírez, J. MicroRNAs Encoded by Virus and Small RNAs Encoded by Bacteria Associated with Oncogenic Processes. Processes 2021, 9, 2234. [Google Scholar] [CrossRef]
- Sora, Y.; Wiwanitkit, V. Parasitic Infections and Cancer: A Status Report. Indian J. Med. Paediatr. Oncol. 2019, 40, 172–174. [Google Scholar] [CrossRef]
- Centre International de Recherche sur le Cancer (Ed.) A Review of Human Carcinogens; IARC Monographs on the Evaluation of Carcinogenic Risks to Humans; International Agency for Research on Cancer: Lyon, France, 2012; ISBN 978-92-832-1329-1. [Google Scholar]
- List of Classifications—IARC Monographs on the Identification of Carcinogenic Hazards to Humans. Available online: https://monographs.iarc.who.int/list-of-classifications (accessed on 17 June 2022).
- Ali Syeda, Z.; Langden, S.S.S.; Munkhzul, C.; Lee, M.; Song, S.J. Regulatory Mechanism of MicroRNA Expression in Cancer. Int. J. Mol. Sci. 2020, 21, E1723. [Google Scholar] [CrossRef] [Green Version]
- Bahrami, A.; Jafari, A.; Ferns, G.A. The Dual Role of MicroRNA-9 in Gastrointestinal Cancers: OncomiR or Tumor Suppressor? Biomed. Pharmacother. 2022, 145, 112394. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Du, L.; Liu, Q.; Lu, Z. MicroRNAs: Novel Players in the Diagnosis and Treatment of Cancer Cachexia (Review). Exp. Ther. Med. 2022, 24, 446. [Google Scholar] [CrossRef] [PubMed]
- Rojas-Pirela, M.; Andrade-Alviárez, D.; Medina, L.; Castillo, C.; Liempi, A.; Guerrero-Muñoz, J.; Ortega, Y.; Maya, J.D.; Rojas, V.; Quiñones, W.; et al. MicroRNAs: Master Regulators in Host-Parasitic Protist Interactions. Open Biol. 2022, 12, 210395. [Google Scholar] [CrossRef] [PubMed]
- Saliminejad, K.; Khorram Khorshid, H.R.; Soleymani Fard, S.; Ghaffari, S.H. An Overview of MicroRNAs: Biology, Functions, Therapeutics, and Analysis Methods. J. Cell. Physiol. 2019, 234, 5451–5465. [Google Scholar] [CrossRef] [PubMed]
- Tribolet, L.; Kerr, E.; Cowled, C.; Bean, A.G.D.; Stewart, C.R.; Dearnley, M.; Farr, R.J. MicroRNA Biomarkers for Infectious Diseases: From Basic Research to Biosensing. Front. Microbiol. 2020, 11, 1197. [Google Scholar] [CrossRef]
- Parizi, P.K.; Yarahmadi, F.; Tabar, H.M.; Hosseini, Z.; Sarli, A.; Kia, N.; Tafazoli, A.; Esmaeili, S.-A. MicroRNAs and Target Molecules in Bladder Cancer. Med. Oncol. Northwood Lond. Engl. 2020, 37, 118. [Google Scholar] [CrossRef]
- Jarroux, J.; Morillon, A.; Pinskaya, M. History, Discovery, and Classification of LncRNAs. Adv. Exp. Med. Biol. 2017, 1008, 1–46. [Google Scholar] [CrossRef]
- Statello, L.; Guo, C.-J.; Chen, L.-L.; Huarte, M. Gene Regulation by Long Non-Coding RNAs and Its Biological Functions. Nat. Rev. Mol. Cell Biol. 2021, 22, 96–118. [Google Scholar] [CrossRef] [PubMed]
- Sun, Q.; Hao, Q.; Prasanth, K.V. Nuclear Long Noncoding RNAs: Key Regulators of Gene Expression. Trends Genet. TIG 2018, 34, 142–157. [Google Scholar] [CrossRef] [PubMed]
- Fang, Y.; Fullwood, M.J. Roles, Functions, and Mechanisms of Long Non-Coding RNAs in Cancer. Genom. Proteom. Bioinform. 2016, 14, 42–54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ahmad, P.; Bensaoud, C.; Mekki, I.; Rehman, M.U.; Kotsyfakis, M. Long Non-Coding RNAs and Their Potential Roles in the Vector-Host-Pathogen Triad. Life 2021, 11, 56. [Google Scholar] [CrossRef]
- Cheng, J.-T.; Wang, L.; Wang, H.; Tang, F.-R.; Cai, W.-Q.; Sethi, G.; Xin, H.-W.; Ma, Z. Insights into Biological Role of LncRNAs in Epithelial-Mesenchymal Transition. Cells 2019, 8, E1178. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Wang, W.; Zhu, W.; Dong, J.; Cheng, Y.; Yin, Z.; Shen, F. Mechanisms and Functions of Long Non-Coding RNAs at Multiple Regulatory Levels. Int. J. Mol. Sci. 2019, 20, E5573. [Google Scholar] [CrossRef] [Green Version]
- Yang, M.; Lu, H.; Liu, J.; Wu, S.; Kim, P.; Zhou, X. LncRNAfunc: A Knowledgebase of LncRNA Function in Human Cancer. Nucleic Acids Res. 2022, 50, D1295–D1306. [Google Scholar] [CrossRef]
- Scholte, L.L.S.; Pascoal-Xavier, M.A.; Nahum, L.A. Helminths and Cancers from the Evolutionary Perspective. Front. Med. 2018, 5, 90. [Google Scholar] [CrossRef] [Green Version]
- Fried, B.; Reddy, A.; Mayer, D. Helminths in Human Carcinogenesis. Cancer Lett. 2011, 305, 239–249. [Google Scholar] [CrossRef]
- Mayer, D.A.; Fried, B. The Role of Helminth Infections in Carcinogenesis. Adv. Parasitol. 2007, 65, 239–296. [Google Scholar] [CrossRef]
- Oikonomopoulou, K.; Brinc, D.; Hadjisavvas, A.; Christofi, G.; Kyriacou, K.; Diamandis, E.P. The Bifacial Role of Helminths in Cancer: Involvement of Immune and Non-Immune Mechanisms. Crit. Rev. Clin. Lab. Sci. 2014, 51, 138–148. [Google Scholar] [CrossRef] [PubMed]
- van Tong, H.; Brindley, P.J.; Meyer, C.G.; Velavan, T.P. Parasite Infection, Carcinogenesis and Human Malignancy. EBioMedicine 2017, 15, 12–23. [Google Scholar] [CrossRef] [PubMed]
- Messina, C.M.; Pizzo, F.; Santulli, A.; Bušelić, I.; Boban, M.; Orhanović, S.; Mladineo, I. Anisakis Pegreffii (Nematoda: Anisakidae) Products Modulate Oxidative Stress and Apoptosis-Related Biomarkers in Human Cell Lines. Parasit. Vectors 2016, 9, 607. [Google Scholar] [CrossRef] [Green Version]
- Sofronic-Milosavljevic, L.; Ilic, N.; Pinelli, E.; Gruden-Movsesijan, A. Secretory Products of Trichinella Spiralis Muscle Larvae and Immunomodulation: Implication for Autoimmune Diseases, Allergies, and Malignancies. J. Immunol. Res. 2015, 2015, 523875. [Google Scholar] [CrossRef] [Green Version]
- Hatta, M.N.A.; Mohamad Hanif, E.A.; Chin, S.-F.; Neoh, H.-M. Pathogens and Carcinogenesis: A Review. Biology 2021, 10, 533. [Google Scholar] [CrossRef]
- Santos, L.L.; Santos, J.; Gouveia, M.J.; Bernardo, C.; Lopes, C.; Rinaldi, G.; Brindley, P.J.; Costa, J.M.C. da Urogenital Schistosomiasis-History, Pathogenesis, and Bladder Cancer. J. Clin. Med. 2021, 10, E205. [Google Scholar] [CrossRef]
- Ishida, K.; Hsieh, M.H. Understanding Urogenital Schistosomiasis-Related Bladder Cancer: An Update. Front. Med. 2018, 5, 223. [Google Scholar] [CrossRef] [Green Version]
- Santos, J.; Chaves, J.; Araújo, H.; Vale, N.; Costa, J.M.; Brindley, P.J.; Lopes, C.; Naples, J.; Shiff, C.; Dupret, J.; et al. Comparison of Findings Using Ultrasonography and Cystoscopy in Urogenital Schistosomiasis in a Public Health Centre in Rural Angola. S. Afr. Med. J. 2015, 105, 312–315. [Google Scholar] [CrossRef] [Green Version]
- Adebayo, A.S.; Suryavanshi, M.V.; Bhute, S.; Agunloye, A.M.; Isokpehi, R.D.; Anumudu, C.I.; Shouche, Y.S. The Microbiome in Urogenital Schistosomiasis and Induced Bladder Pathologies. PLoS Negl. Trop. Dis. 2017, 11, e0005826. [Google Scholar] [CrossRef] [Green Version]
- Chala, B.; Choi, M.-H.; Moon, K.C.; Kim, H.S.; Kwak, C.; Hong, S.-T. Development of Urinary Bladder Pre-Neoplasia by Schistosoma Haematobium Eggs and Chemical Carcinogen in Mice. Korean J. Parasitol. 2017, 55, 21–29. [Google Scholar] [CrossRef] [Green Version]
- Honeycutt, J.; Hammam, O.; Fu, C.-L.; Hsieh, M.H. Controversies and Challenges in Research on Urogenital Schistosomiasis-Associated Bladder Cancer. Trends Parasitol. 2014, 30, 324–332. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aly, M.S.; Khaled, H.M.; Emara, M.; Hussein, T.D. Cytogenetic Profile of Locally Advanced and Metastatic Schistosoma-Related Bladder Cancer and Response to Chemotherapy. Cancer Genet. 2012, 205, 156–162. [Google Scholar] [CrossRef] [PubMed]
- Botelho, M.C.; Veiga, I.; Oliveira, P.A.; Lopes, C.; Teixeira, M.; da Costa, J.M.C.; Machado, J.C. Carcinogenic Ability of Schistosoma Haematobium Possibly through Oncogenic Mutation of KRAS Gene. Adv. Cancer Res. Treat. 2013, 2013, 876585. [Google Scholar] [PubMed]
- Hamid, H.K.S. Schistosoma Japonicum-Associated Colorectal Cancer: A Review. Am. J. Trop. Med. Hyg. 2019, 100, 501–505. [Google Scholar] [CrossRef] [Green Version]
- Na, B.-K.; Pak, J.H.; Hong, S.-J. Clonorchis Sinensis and Clonorchiasis. Acta Trop. 2020, 203, 105309. [Google Scholar] [CrossRef]
- Qian, M.-B.; Zhou, X.-N. Clonorchis Sinensis. Trends Parasitol. 2021, 37, 1014–1015. [Google Scholar] [CrossRef]
- Bouvard, V.; Baan, R.; Straif, K.; Grosse, Y.; Secretan, B.; El Ghissassi, F.; Benbrahim-Tallaa, L.; Guha, N.; Freeman, C.; Galichet, L.; et al. A Review of Human Carcinogens--Part B: Biological Agents. Lancet Oncol. 2009, 10, 321–322. [Google Scholar] [CrossRef]
- Pak, J.H.; Lee, J.-Y.; Jeon, B.Y.; Dai, F.; Yoo, W.G.; Hong, S.-J. Cytokine Production in Cholangiocarcinoma Cells in Response to Clonorchis Sinensis Excretory-Secretory Products and Their Putative Protein Components. Korean J. Parasitol. 2019, 57, 379–387. [Google Scholar] [CrossRef]
- Won, J.; Cho, Y.; Lee, D.; Jeon, B.Y.; Ju, J.-W.; Chung, S.; Pak, J.H. Clonorchis Sinensis Excretory-Secretory Products Increase Malignant Characteristics of Cholangiocarcinoma Cells in Three-Dimensional Co-Culture with Biliary Ductal Plates. PLoS Pathog. 2019, 15, e1007818. [Google Scholar] [CrossRef]
- Bahk, Y.Y.; Pak, J.H. Toll-Like Receptor-Mediated Free Radical Generation in Clonorchis Sinensis Excretory-Secretory Product-Treated Cholangiocarcinoma Cells. Korean J. Parasitol. 2016, 54, 679–684. [Google Scholar] [CrossRef]
- Nam, J.-H.; Moon, J.H.; Kim, I.K.; Lee, M.-R.; Hong, S.-J.; Ahn, J.H.; Chung, J.W.; Pak, J.H. Free Radicals Enzymatically Triggered by Clonorchis Sinensis Excretory-Secretory Products Cause NF-ΚB-Mediated Inflammation in Human Cholangiocarcinoma Cells. Int. J. Parasitol. 2012, 42, 103–113. [Google Scholar] [CrossRef] [PubMed]
- Sripa, B.; Brindley, P.J.; Mulvenna, J.; Laha, T.; Smout, M.J.; Mairiang, E.; Bethony, J.M.; Loukas, A. The Tumorigenic Liver Fluke Opisthorchis Viverrini--Multiple Pathways to Cancer. Trends Parasitol. 2012, 28, 395–407. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jusakul, A.; Kongpetch, S.; Teh, B.T. Genetics of Opisthorchis Viverrini-Related Cholangiocarcinoma. Curr. Opin. Gastroenterol. 2015, 31, 258–263. [Google Scholar] [CrossRef] [PubMed]
- Stroehlein, A.J.; Young, N.D.; Korhonen, P.K.; Hall, R.S.; Jex, A.R.; Webster, B.L.; Rollinson, D.; Brindley, P.J.; Gasser, R.B. The Small RNA Complement of Adult Schistosoma Haematobium. PLoS Negl. Trop. Dis. 2018, 12, e0006535. [Google Scholar] [CrossRef] [PubMed]
- Cardoso, T.C.; de, S.; de Araújo, C.B.; Portilho, L.G.; Mendes, L.G.A.; Alves, T.C.; Silva, G.C.; Ribeiro, T.H.C.; Gandolfi, P.E.; Morais, E.R.; et al. Computational Prediction and Characterisation of MiRNAs and Their Pathway Genes in Human Schistosomiasis Caused by Schistosoma Haematobium. Mem. Inst. Oswaldo Cruz 2020, 115, e190378. [Google Scholar] [CrossRef] [PubMed]
- Meningher, T.; Lerman, G.; Regev-Rudzki, N.; Gold, D.; Ben-Dov, I.Z.; Sidi, Y.; Avni, D.; Schwartz, E. Schistosomal MicroRNAs Isolated From Extracellular Vesicles in Sera of Infected Patients: A New Tool for Diagnosis and Follow-up of Human Schistosomiasis. J. Infect. Dis. 2017, 215, 378–386. [Google Scholar] [CrossRef]
- Gaber, D.A.; Wassef, R.M.; El-Ayat, W.M.; El-Moazen, M.I.; Montasser, K.A.; Swar, S.A.; Amin, H.A.A. Role of a Schistosoma Haematobium Specific MicroRNA as a Predictive and Prognostic Tool for Bilharzial Bladder Cancer in Egypt. Sci. Rep. 2020, 10, 18844. [Google Scholar] [CrossRef]
- Grilo, I.; Rodrigues, C.; Soares, A.; Grande, E. Facing Treatment of Non-Urothelial Bladder Cancers in the Immunotherapy Era. Crit. Rev. Oncol. Hematol. 2020, 153, 103034. [Google Scholar] [CrossRef]
- Lopez-Beltran, A.; Henriques, V.; Montironi, R.; Cimadamore, A.; Raspollini, M.R.; Cheng, L. Variants and New Entities of Bladder Cancer. Histopathology 2019, 74, 77–96. [Google Scholar] [CrossRef] [Green Version]
- Sirekbasan, S.; Gurkok Tan, T. In Silico Analysis of Common Long Noncoding RNAs in Schistosoma Mansoni and Schistosoma Haematobium. J. Trop. Med. 2021, 2021, 6617118. [Google Scholar] [CrossRef]
- Cai, P.; Hou, N.; Piao, X.; Liu, S.; Liu, H.; Yang, F.; Wang, J.; Jin, Q.; Wang, H.; Chen, Q. Profiles of Small Non-Coding RNAs in Schistosoma Japonicum during Development. PLoS Negl. Trop. Dis. 2011, 5, e1256. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, J.; Yu, Y.; Li, Q.; Chen, M.; Shen, H.; Zhang, R.; Song, M.; Hu, W. Comprehensive Analysis of MiRNA Profiles Reveals the Role of Schistosoma Japonicum MiRNAs at Different Developmental Stages. Vet. Res. 2019, 50, 23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Z.; Xue, X.; Sun, J.; Luo, R.; Xu, X.; Jiang, Y.; Zhang, Q.; Pan, W. An “in-Depth” Description of the Small Non-Coding RNA Population of Schistosoma Japonicum Schistosomulum. PLoS Negl. Trop. Dis. 2010, 4, e596. [Google Scholar] [CrossRef] [PubMed]
- Cai, P.; Liu, S.; Piao, X.; Hou, N.; Gobert, G.N.; McManus, D.P.; Chen, Q. Comprehensive Transcriptome Analysis of Sex-Biased Expressed Genes Reveals Discrete Biological and Physiological Features of Male and Female Schistosoma Japonicum. PLoS Negl. Trop. Dis. 2016, 10, e0004684. [Google Scholar] [CrossRef] [Green Version]
- Huang, J.; Hao, P.; Chen, H.; Hu, W.; Yan, Q.; Liu, F.; Han, Z.-G. Genome-Wide Identification of Schistosoma Japonicum MicroRNAs Using a Deep-Sequencing Approach. PLoS ONE 2009, 4, e8206. [Google Scholar] [CrossRef]
- Xue, X.; Sun, J.; Zhang, Q.; Wang, Z.; Huang, Y.; Pan, W. Identification and Characterization of Novel MicroRNAs from Schistosoma Japonicum. PLoS ONE 2008, 3, e4034. [Google Scholar] [CrossRef] [Green Version]
- Cheng, G.; Jin, Y. MicroRNAs: Potentially Important Regulators for Schistosome Development and Therapeutic Targets against Schistosomiasis. Parasitology 2012, 139, 669–679. [Google Scholar] [CrossRef]
- Zhao, J.; Luo, R.; Xu, X.; Zou, Y.; Zhang, Q.; Pan, W. High-Throughput Sequencing of RNAs Isolated by Cross-Linking Immunoprecipitation (HITS-CLIP) Reveals Argonaute-Associated MicroRNAs and Targets in Schistosoma Japonicum. Parasit. Vectors 2015, 8, 589. [Google Scholar] [CrossRef] [Green Version]
- Hao, L.; Cai, P.; Jiang, N.; Wang, H.; Chen, Q. Identification and Characterization of MicroRNAs and Endogenous SiRNAs in Schistosoma Japonicum. BMC Genom. 2010, 11, 55. [Google Scholar] [CrossRef] [Green Version]
- Zhu, L.; Zhao, J.; Wang, J.; Hu, C.; Peng, J.; Luo, R.; Zhou, C.; Liu, J.; Lin, J.; Jin, Y.; et al. MicroRNAs Are Involved in the Regulation of Ovary Development in the Pathogenic Blood Fluke Schistosoma Japonicum. PLoS Pathog. 2016, 12, e1005423. [Google Scholar] [CrossRef] [Green Version]
- Han, Y.; Feng, J.; Ren, Y.; Wu, L.; Li, H.; Liu, J.; Jin, Y. Differential Expression of MicroRNA between Normally Developed and Underdeveloped Female Worms of Schistosoma Japonicum. Vet. Res. 2020, 51, 126. [Google Scholar] [CrossRef] [PubMed]
- Sun, J.; Wang, S.; Li, C.; Ren, Y.; Wang, J. Novel Expression Profiles of MicroRNAs Suggest That Specific MiRNAs Regulate Gene Expression for the Sexual Maturation of Female Schistosoma Japonicum after Pairing. Parasit. Vectors 2014, 7, 177. [Google Scholar] [CrossRef] [Green Version]
- Sun, J.; Wang, S.-W.; Li, C. ATP Synthase: An Identified Target Gene of Bantam in Paired Female Schistosoma Japonicum. Parasitol. Res. 2015, 114, 593–600. [Google Scholar] [CrossRef] [PubMed]
- Ai, L.; Hu, W.; Zhang, R.L.; Huang, D.N.; Chen, S.H.; Xu, B.; Li, H.; Cai, Y.C.; Lu, Y.; Zhou, X.N.; et al. MicroRNAs Expression Profiles in Schistosoma Japonicum of Different Sex 14 and 28 Days Post-Infection. Trop. Biomed. 2020, 37, 947–962. [Google Scholar] [CrossRef] [PubMed]
- Du, P.; Giri, B.R.; Liu, J.; Xia, T.; Grevelding, C.G.; Cheng, G. Proteomic and Deep Sequencing Analysis of Extracellular Vesicles Isolated from Adult Male and Female Schistosoma Japonicum. PLoS Negl. Trop. Dis. 2020, 14, e0008618. [Google Scholar] [CrossRef]
- Zhu, L.; Liu, J.; Dao, J.; Lu, K.; Li, H.; Gu, H.; Liu, J.; Feng, X.; Cheng, G. Molecular Characterization of S. Japonicum Exosome-like Vesicles Reveals Their Regulatory Roles in Parasite-Host Interactions. Sci. Rep. 2016, 6, 25885. [Google Scholar] [CrossRef]
- Kumagai, T.; Shimogawara, R.; Ichimura, K.; Iwanaga, S. Calpain Inhibitor Suppresses Both Extracellular Vesicle-Mediated Secretion of MiRNAs and Egg Production from Paired Adults of Schistosoma Japonicum. Parasitol. Int. 2022, 87, 102540. [Google Scholar] [CrossRef]
- Han, H.; Peng, J.; Hong, Y.; Fu, Z.; Lu, K.; Li, H.; Zhu, C.; Zhao, Q.; Lin, J. Comparative Analysis of MicroRNA in Schistosomula Isolated from Non-Permissive Host and Susceptible Host. Mol. Biochem. Parasitol. 2015, 204, 81–88. [Google Scholar] [CrossRef]
- Han, H.; Peng, J.; Hong, Y.; Fu, Z.; Lu, K.; Li, H.; Zhu, C.; Zhao, Q.; Lin, J. Comparative Characterization of MicroRNAs in Schistosoma Japonicum Schistosomula from Wistar Rats and BALB/c Mice. Parasitol. Res. 2015, 114, 2639–2647. [Google Scholar] [CrossRef]
- Yu, X.; Zhai, Q.; Fu, Z.; Hong, Y.; Liu, J.; Li, H.; Lu, K.; Zhu, C.; Lin, J.; Li, G. Comparative Analysis of MicroRNA Expression Profiles of Adult Schistosoma Japonicum Isolated from Water Buffalo and Yellow Cattle. Parasit. Vectors 2019, 12, 196. [Google Scholar] [CrossRef]
- Liu, R.; Zhong, Q.-P.; Tang, H.-B.; Dong, H.-F. Comparative Characterization of MicroRNAs of Schistosoma Japonicum from SCID Mice and BALB/c Mice: Clues to the Regulation of Parasite Growth and Development. Acta Trop. 2022, 225, 106200. [Google Scholar] [CrossRef] [PubMed]
- He, X.; Wang, Y.; Fan, X.; Lei, N.; Tian, Y.; Zhang, D.; Pan, W. A Schistosome MiRNA Promotes Host Hepatic Fibrosis by Targeting Transforming Growth Factor Beta Receptor III. J. Hepatol. 2020, 72, 519–527. [Google Scholar] [CrossRef] [PubMed]
- Cai, P.; Piao, X.; Hao, L.; Liu, S.; Hou, N.; Wang, H.; Chen, Q. A Deep Analysis of the Small Non-Coding RNA Population in Schistosoma Japonicum Eggs. PLoS ONE 2013, 8, e64003. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cheng, G.; Luo, R.; Hu, C.; Cao, J.; Jin, Y. Deep Sequencing-Based Identification of Pathogen-Specific MicroRNAs in the Plasma of Rabbits Infected with Schistosoma Japonicum. Parasitology 2013, 140, 1751–1761. [Google Scholar] [CrossRef]
- Zhu, S.; Wang, S.; Lin, Y.; Jiang, P.; Cui, X.; Wang, X.; Zhang, Y.; Pan, W. Release of Extracellular Vesicles Containing Small RNAs from the Eggs of Schistosoma Japonicum. Parasit. Vectors 2016, 9, 574. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Liao, Y.; Yang, R.; Yu, Z.; Zhang, L.; Zhu, Z.; Wu, X.; Shen, J.; Liu, J.; Xu, L.; et al. Sja-MiR-71a in Schistosome Egg-Derived Extracellular Vesicles Suppresses Liver Fibrosis Caused by Schistosomiasis via Targeting Semaphorin 4D. J. Extracell. Vesicles 2020, 9, 1785738. [Google Scholar] [CrossRef]
- Wang, Y.; Fan, X.; Lei, N.; He, X.; Wang, X.; Luo, X.; Zhang, D.; Pan, W. A MicroRNA Derived From Schistosoma Japonicum Promotes Schistosomiasis Hepatic Fibrosis by Targeting Host Secreted Frizzled-Related Protein 1. Front. Cell. Infect. Microbiol. 2020, 10, 101. [Google Scholar] [CrossRef]
- Dhar, D.; Baglieri, J.; Kisseleva, T.; Brenner, D.A. Mechanisms of Liver Fibrosis and Its Role in Liver Cancer. Exp. Biol. Med. Maywood NJ 2020, 245, 96–108. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.; Zhu, L.; Wang, J.; Qiu, L.; Chen, Y.; Davis, R.E.; Cheng, G. Schistosoma Japonicum Extracellular Vesicle MiRNA Cargo Regulates Host Macrophage Functions Facilitating Parasitism. PLoS Pathog. 2019, 15, e1007817. [Google Scholar] [CrossRef] [Green Version]
- Meningher, T.; Barsheshet, Y.; Ofir-Birin, Y.; Gold, D.; Brant, B.; Dekel, E.; Sidi, Y.; Schwartz, E.; Regev-Rudzki, N.; Avni, O.; et al. Schistosomal Extracellular Vesicle-Enclosed MiRNAs Modulate Host T Helper Cell Differentiation. EMBO Rep. 2020, 21, e47882. [Google Scholar] [CrossRef]
- Hu, C.; Li, Y.; Pan, D.; Wang, J.; Zhu, L.; Lin, Y.; Zhu, S.; Pan, W. A Schistosoma Japonicum MicroRNA Exerts Antitumor Effects Through Inhibition of Both Cell Migration and Angiogenesis by Targeting PGAM1. Front. Oncol. 2021, 11, 652395. [Google Scholar] [CrossRef] [PubMed]
- Hu, C.; Zhu, S.; Wang, J.; Lin, Y.; Ma, L.; Zhu, L.; Jiang, P.; Li, Z.; Pan, W. Schistosoma Japonicum MiRNA-7-5p Inhibits the Growth and Migration of Hepatoma Cells via Cross-Species Regulation of S-Phase Kinase-Associated Protein 2. Front. Oncol. 2019, 9, 175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, P.; Wang, J.; Zhu, S.; Hu, C.; Lin, Y.; Pan, W. Identification of a Schistosoma Japonicum MicroRNA That Suppresses Hepatoma Cell Growth and Migration by Targeting Host FZD4 Gene. Front. Cell. Infect. Microbiol. 2022, 12, 786543. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.; Zhu, S.; Hu, C.; Wang, J.; Jiang, P.; Zhu, L.; Li, Z.; Wang, S.; Zhang, Y.; Xu, X.; et al. Cross-Species Suppression of Hepatoma Cell Growth and Migration by a Schistosoma Japonicum MicroRNA. Mol. Ther. Nucleic Acids 2019, 18, 400–412. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, S.; Giri, B.R.; Liu, J.; He, X.; Cai, P.; Jing, Z.; Cheng, G. Characterization of MicroRNA Cargo of Extracellular Vesicles Isolated from the Plasma of Schistosoma Japonicum-Infected Mice. Front. Cell. Infect. Microbiol. 2022, 12, 803242. [Google Scholar] [CrossRef] [PubMed]
- Cai, P.; Gobert, G.N.; You, H.; Duke, M.; McManus, D.P. Circulating MiRNAs: Potential Novel Biomarkers for Hepatopathology Progression and Diagnosis of Schistosomiasis Japonica in Two Murine Models. PLoS Negl. Trop. Dis. 2015, 9, e0003965. [Google Scholar] [CrossRef] [Green Version]
- Mu, Y.; Cai, P.; Olveda, R.M.; Ross, A.G.; Olveda, D.U.; McManus, D.P. Parasite-Derived Circulating MicroRNAs as Biomarkers for the Detection of Human Schistosoma Japonicum Infection. Parasitology 2020, 147, 889–896. [Google Scholar] [CrossRef]
- Liao, Q.; Zhang, Y.; Zhu, Y.; Chen, J.; Dong, C.; Tao, Y.; He, A.; Liu, J.; Wu, Z. Identification of Long Noncoding RNAs in Schistosoma Mansoni and Schistosoma Japonicum. Exp. Parasitol. 2018, 191, 82–87. [Google Scholar] [CrossRef]
- Maciel, L.F.; Morales-Vicente, D.A.; Verjovski-Almeida, S. Dynamic Expression of Long Non-Coding RNAs Throughout Parasite Sexual and Neural Maturation in Schistosoma Japonicum. NonCoding RNA 2020, 6, E15. [Google Scholar] [CrossRef] [Green Version]
- Xu, M.-J.; Liu, Q.; Nisbet, A.J.; Cai, X.-Q.; Yan, C.; Lin, R.-Q.; Yuan, Z.-G.; Song, H.-Q.; He, X.-H.; Zhu, X.-Q. Identification and Characterization of MicroRNAs in Clonorchis Sinensis of Human Health Significance. BMC Genom. 2010, 11, 521. [Google Scholar] [CrossRef] [Green Version]
- Ovchinnikov, V.Y.; Afonnikov, D.A.; Vasiliev, G.V.; Kashina, E.V.; Sripa, B.; Mordvinov, V.A.; Katokhin, A.V. Identification of MicroRNA Genes in Three Opisthorchiids. PLoS Negl. Trop. Dis. 2015, 9, e0003680. [Google Scholar] [CrossRef] [PubMed]
- Ovchinnikov, V.Y.; Mordvinov, V.A.; Fromm, B. Extreme Conservation of MiRNA Complements in Opisthorchiids. Parasitol. Int. 2017, 66, 773–776. [Google Scholar] [CrossRef] [PubMed]
- Stark, V.A.; Facey, C.O.B.; Viswanathan, V.; Boman, B.M. The Role of MiRNAs, MiRNA Clusters, and IsomiRs in Development of Cancer Stem Cell Populations in Colorectal Cancer. Int. J. Mol. Sci. 2021, 22, 1424. [Google Scholar] [CrossRef]
- Yan, C.; Zhou, Q.-Y.; Wu, J.; Xu, N.; Du, Y.; Li, J.; Liu, J.-X.; Koda, S.; Zhang, B.-B.; Yu, Q.; et al. Csi-Let-7a-5p Delivered by Extracellular Vesicles from a Liver Fluke Activates M1-like Macrophages and Exacerbates Biliary Injuries. Proc. Natl. Acad. Sci. USA 2021, 118, e2102206118. [Google Scholar] [CrossRef] [PubMed]
- Brindley, P.J.; Bachini, M.; Ilyas, S.I.; Khan, S.A.; Loukas, A.; Sirica, A.E.; Teh, B.T.; Wongkham, S.; Gores, G.J. Cholangiocarcinoma. Nat. Rev. Dis. Primer 2021, 7, 65. [Google Scholar] [CrossRef]
- Young, N.D.; Nagarajan, N.; Lin, S.J.; Korhonen, P.K.; Jex, A.R.; Hall, R.S.; Safavi-Hemami, H.; Kaewkong, W.; Bertrand, D.; Gao, S.; et al. The Opisthorchis Viverrini Genome Provides Insights into Life in the Bile Duct. Nat. Commun. 2014, 5, 4378. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Gong, W.; Cao, S.; Yin, J.; Zhang, J.; Cao, J.; Shen, Y. Comprehensive Analysis of Non-Coding RNA Profiles of Exosome-Like Vesicles from the Protoscoleces and Hydatid Cyst Fluid of Echinococcus Granulosus. Front. Cell. Infect. Microbiol. 2020, 10, 316. [Google Scholar] [CrossRef]
- de Souza Gomes, M.; Muniyappa, M.K.; Carvalho, S.G.; Guerra-Sá, R.; Spillane, C. Genome-Wide Identification of Novel MicroRNAs and Their Target Genes in the Human Parasite Schistosoma Mansoni. Genomics 2011, 98, 96–111. [Google Scholar] [CrossRef] [Green Version]
- Manzano-Román, R.; Siles-Lucas, M. MicroRNAs in Parasitic Diseases: Potential for Diagnosis and Targeting. Mol. Biochem. Parasitol. 2012, 186, 81–86. [Google Scholar] [CrossRef]
- Kim, T.-S.; Pak, J.H.; Kim, J.-B.; Bahk, Y.Y. Clonorchis Sinensis, an Oriental Liver Fluke, as a Human Biological Agent of Cholangiocarcinoma: A Brief Review. BMB Rep. 2016, 49, 590–597. [Google Scholar] [CrossRef] [Green Version]
- Prueksapanich, P.; Piyachaturawat, P.; Aumpansub, P.; Ridtitid, W.; Chaiteerakij, R.; Rerknimitr, R. Liver Fluke-Associated Biliary Tract Cancer. Gut Liver 2018, 12, 236–245. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chaiyadet, S.; Sotillo, J.; Smout, M.; Cantacessi, C.; Jones, M.K.; Johnson, M.S.; Turnbull, L.; Whitchurch, C.B.; Potriquet, J.; Laohaviroj, M.; et al. Carcinogenic Liver Fluke Secretes Extracellular Vesicles That Promote Cholangiocytes to Adopt a Tumorigenic Phenotype. J. Infect. Dis. 2015, 212, 1636–1645. [Google Scholar] [CrossRef]
- Dangtakot, R.; Intuyod, K.; Chamgramol, Y.; Pairojkul, C.; Pinlaor, S.; Jantawong, C.; Pongking, T.; Haonon, O.; Ma, N.; Pinlaor, P. CagA+ Helicobacter Pylori Infection and N-Nitrosodimethylamine Administration Induce Cholangiocarcinoma Development in Hamsters. Helicobacter 2021, 26, e12817. [Google Scholar] [CrossRef] [PubMed]
- Pakharukova, M.Y.; Zaparina, O.; Hong, S.-J.; Sripa, B.; Mordvinov, V.A. A Comparative Study of Helicobacter Pylori Infection in Hamsters Experimentally Infected with Liver Flukes Opisthorchis Felineus, Opisthorchis Viverrini, or Clonorchis Sinensis. Sci. Rep. 2021, 11, 7789. [Google Scholar] [CrossRef] [PubMed]
- Boonyanugomol, W.; Chomvarin, C.; Sripa, B.; Bhudhisawasdi, V.; Khuntikeo, N.; Hahnvajanawong, C.; Chamsuwan, A. Helicobacter Pylori in Thai Patients with Cholangiocarcinoma and Its Association with Biliary Inflammation and Proliferation. HPB 2012, 14, 177–184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Deenonpoe, R.; Chomvarin, C.; Pairojkul, C.; Chamgramol, Y.; Loukas, A.; Brindley, P.J.; Sripa, B. The Carcinogenic Liver Fluke Opisthorchis Viverrini Is a Reservoir for Species of Helicobacter. Asian Pac. J. Cancer Prev. APJCP 2015, 16, 1751–1758. [Google Scholar] [CrossRef] [Green Version]
- Deenonpoe, R.; Mairiang, E.; Mairiang, P.; Pairojkul, C.; Chamgramol, Y.; Rinaldi, G.; Loukas, A.; Brindley, P.J.; Sripa, B. Elevated Prevalence of Helicobacter Species and Virulence Factors in Opisthorchiasis and Associated Hepatobiliary Disease. Sci. Rep. 2017, 7, 42744. [Google Scholar] [CrossRef]
- Dheilly, N.M.; Ewald, P.W.; Brindley, P.J.; Fichorova, R.N.; Thomas, F. Parasite-Microbe-Host Interactions and Cancer Risk. PLoS Pathog. 2019, 15, e1007912. [Google Scholar] [CrossRef] [Green Version]
- Li, R.; Hu, Z.; Wang, Z.; Zhu, T.; Wang, G.; Gao, B.; Wang, J.; Deng, X. MiR-125a-5p Promotes Gastric Cancer Growth and Invasion by Regulating the Hippo Pathway. J. Clin. Lab. Anal. 2021, 35, e24078. [Google Scholar] [CrossRef]
- Beilerli, A.; Gareev, I.; Beylerli, O.; Yang, G.; Pavlov, V.; Aliev, G.; Ahmad, A. Circular RNAs as Biomarkers and Therapeutic Targets in Cancer. Semin. Cancer Biol. 2022, 83, 242–252. [Google Scholar] [CrossRef]
- Minkler, S.J.; Loghry-Jansen, H.J.; Sondjaja, N.A.; Kimber, M.J. Expression and Secretion of Circular RNAs in the Parasitic Nematode, Ascaris Suum. Front. Genet. 2022, 13, 884052. [Google Scholar] [CrossRef] [PubMed]
- Zhou, C.; Zhang, Y.; Wu, S.; Wang, Z.; Tuersong, W.; Wang, C.; Liu, F.; Hu, M. Genome-Wide Identification of CircRNAs of Infective Larvae and Adult Worms of Parasitic Nematode, Haemonchus Contortus. Front. Cell. Infect. Microbiol. 2021, 11, 764089. [Google Scholar] [CrossRef] [PubMed]
- Cortés-López, M.; Gruner, M.R.; Cooper, D.A.; Gruner, H.N.; Voda, A.-I.; van der Linden, A.M.; Miura, P. Global Accumulation of CircRNAs during Aging in Caenorhabditis Elegans. BMC Genom. 2018, 19, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
miRNA | Host Molecular Target | Model | Biological Effect | Possible Seed Sequence | Ref ‡ |
---|---|---|---|---|---|
Sja-mir-61 | PGAM1 | Liver tumor cells Xenograft tumor mouse model | Inhibition of cell migration Inhibition of cell growth | 5′-GACUAGA-3′ | [93] |
Sja-mir-7-5p | SKP2 | Liver tumor cells Xenograft tumor mouse model | Inhibition of cell proliferation Arrest of cell cycle Inhibition of cell migration | 5′-UGGAAGA-3′ | [94] |
Sja-mir-71a | FZD4 | Liver tumor cells Xenograft tumor mouse model | Inhibition of cell proliferation Arrest of cell cycle Inhibition of cell migration | 5′-GAAAGAC-3′ | [95] |
Sja-mir-3096 | PIK3C2A | Liver tumor cells Xenograft tumor mouse model | Inhibition of cell proliferation Inhibition of cell migration Arrest of cell cycle | 5′-UGGACCA-3′ | [96] |
Sja-mir-3005; Sja-mir-3006; Sja-mir-3044; Sja-mir-7; Sja-mir-124 | ND * | Liver tumor cells | Arrest of cell cycle | --------------- | [95,96] |
miRNA | Host Molecular Target | Biological Effect | Possible Seed Sequence | Ref ‡ |
---|---|---|---|---|
Sha-mir-71a | MAPK-3 | ND * Found in urine of bladder cancer patients associated with infection | 5′-GAAAGAC-3′ | [56,59,110] |
Sja-mir-1 | SFRP1 ¥ | Promotion of hepatic fibrosis and activation of HSC | 5′-GGAAUGU-3′ | [89] |
Sja-mir-2162 | TGFβ3 ¥ | Promotion of hepatic fibrosis and activation of HSC | 5′-UAUUAUGCA-3′ | [84] |
Sja-mir-125b, Sja-mir-219, Sja-mir-923, Sja-mir-3482 and Sja-mir-3480 | ND * | Activation of HSC | --------- | [84] |
Sja-mir-125b | 257 predicted putative targets PROS1 ¥ | Promotion of inflammation Macrophage polarization | 5′-UCCCUGAGA-3′ | [64,68,84,91] |
Sja-bantam | 12 predicted putative targets FAM212B ¥ and CLMP ¥ | Promotion of inflammation Macrophage polarization | 5′-GAGAUCG-3′ | [91] |
Csi-let-7a-5p | SOCS1 ¥ and CLEC7A ¥ | Promotion of inflammation Macrophage polarization Biliary injury | 5′-GAGGUAG-3′ | [106] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Leija-Montoya, A.G.; González-Ramírez, J.; Martínez-Coronilla, G.; Mejía-León, M.E.; Isiordia-Espinoza, M.; Sánchez-Muñoz, F.; Chávez-Cortez, E.G.; Pitones-Rubio, V.; Serafín-Higuera, N. Roles of microRNAs and Long Non-Coding RNAs Encoded by Parasitic Helminths in Human Carcinogenesis. Int. J. Mol. Sci. 2022, 23, 8173. https://doi.org/10.3390/ijms23158173
Leija-Montoya AG, González-Ramírez J, Martínez-Coronilla G, Mejía-León ME, Isiordia-Espinoza M, Sánchez-Muñoz F, Chávez-Cortez EG, Pitones-Rubio V, Serafín-Higuera N. Roles of microRNAs and Long Non-Coding RNAs Encoded by Parasitic Helminths in Human Carcinogenesis. International Journal of Molecular Sciences. 2022; 23(15):8173. https://doi.org/10.3390/ijms23158173
Chicago/Turabian StyleLeija-Montoya, Ana Gabriela, Javier González-Ramírez, Gustavo Martínez-Coronilla, María Esther Mejía-León, Mario Isiordia-Espinoza, Fausto Sánchez-Muñoz, Elda Georgina Chávez-Cortez, Viviana Pitones-Rubio, and Nicolas Serafín-Higuera. 2022. "Roles of microRNAs and Long Non-Coding RNAs Encoded by Parasitic Helminths in Human Carcinogenesis" International Journal of Molecular Sciences 23, no. 15: 8173. https://doi.org/10.3390/ijms23158173