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Muhammad Munir
Division of Biomedical and Life Sciences, Faculty of Health and Medicine, Lancaster University, Lancaster LA1 4YW, UK

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Short Biography

I am a virologist with research experience in virus pathobiology, viral antagonism of immune responses, and host factors that limit virus replication. Research in my laboratory focuses on understanding molecular mechanisms of inter-species pathogenesis of viruses (i.e., zoonotic viruses). Specifically, using influenza viruses and coronaviruses (e.g. SARS-CoV-2, causative agent of CoVID-19), my research aim is to explore host and viral RNA biology (sensing—interferon responses, epigenetics, and gene regulation) and define structural and functional differences in humans and animals (e.g., birds and bats), which determine the transmission dynamics of animal viruses to humans.

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Journal article
Published: 26 August 2021 in Electronics
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An artificial intelligence-assisted low-cost portable device for the rapid detection of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is presented here. This standalone temperature-controlled device houses tubes designed for conducting reverse transcription loop-mediated isothermal amplification (RT-LAMP) assays. Moreover, the device utilises tubes illuminated by LEDs, an in-built camera, and a small onboard computer with automated image acquisition and processing algorithms. This intelligent device significantly reduces the normal assay run time and removes the subjectivity associated with operator interpretation of colourimetric RT-LAMP results. To further improve this device’s usability, a mobile app has been integrated into the system to control the LAMP assay environment and to visually display the assay results by connecting the device to a smartphone via Bluetooth. This study was undertaken using ~5000 images produced from the ~200 LAMP amplification assays using the prototype device. Synthetic RNA and a small panel of positive and negative SARS-CoV-2 patient samples were assayed for this study. State-of-the-art image processing and artificial intelligence algorithms were applied to these images to analyse them and to select the most efficient algorithm. The template matching algorithm for image extraction and MobileNet CNN architecture for classification results provided 98.0% accuracy with an average run time of 20 min to confirm the endpoint result. Two working points were chosen based on the best compromise between sensitivity and specificity. The high sensitivity point has a sensitivity value of 99.12% and specificity value of 70.8%, while at the high specificity point, the sensitivity is 96.05% and specificity 93.59%. Furthermore, this device provides an efficient and cost-effective platform for non-health professionals to detect not only SARS-CoV-2 but also other pathogens in resource-limited laboratories, factories, airports, schools, universities, and homes.

ACS Style

Mukunthan Tharmakulasingam; Nouman S. Chaudhry; Anil Fernando; Manoharanehru Branavan; Wamadeva Balachandran; Aurore C. Poirier; Mohammed A. Rohaim; Muhammad Munir; Roberto M. La Ragione. An Artificial Intelligence-Assisted Portable Low-Cost Device for the Rapid Detection of SARS-CoV-2. Electronics 2021, 10, 2065 .

AMA Style

Mukunthan Tharmakulasingam, Nouman S. Chaudhry, Anil Fernando, Manoharanehru Branavan, Wamadeva Balachandran, Aurore C. Poirier, Mohammed A. Rohaim, Muhammad Munir, Roberto M. La Ragione. An Artificial Intelligence-Assisted Portable Low-Cost Device for the Rapid Detection of SARS-CoV-2. Electronics. 2021; 10 (17):2065.

Chicago/Turabian Style

Mukunthan Tharmakulasingam; Nouman S. Chaudhry; Anil Fernando; Manoharanehru Branavan; Wamadeva Balachandran; Aurore C. Poirier; Mohammed A. Rohaim; Muhammad Munir; Roberto M. La Ragione. 2021. "An Artificial Intelligence-Assisted Portable Low-Cost Device for the Rapid Detection of SARS-CoV-2." Electronics 10, no. 17: 2065.

Journal article
Published: 06 August 2021 in International Journal of Molecular Sciences
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Mammalian cells utilize a wide spectrum of pathways to antagonize the viral replication. These pathways are typically regulated by antiviral proteins and can be constitutively expressed but also exacerbated by interferon induction. A myriad of interferon-stimulated genes (ISGs) have been identified in mounting broad-spectrum antiviral responses. Members of the interferon-induced transmembrane (IFITM) family of proteins are unique among these ISGs due to their ability to prevent virus entry through the lipid bilayer into the cell. In the current study, we generated transgenic chickens that constitutively and stably expressed chicken IFITM1 (chIFITM1) using the avian sarcoma-leukosis virus (RCAS)-based gene transfer system. The challenged transgenic chicks with clinical dose 104 egg infective dose 50 (EID50) of highly pathogenic avian influenza virus (HPAIV) subtype H5N1 (clade 2.2.1.2) showed 100% protection and significant infection tolerance. Although challenged transgenic chicks displayed 60% protection against challenge with the sub-lethal dose (EID50 105), the transgenic chicks showed delayed clinical symptoms, reduced virus shedding, and reduced histopathologic alterations compared to non-transgenic challenged control chickens. These finding indicate that the sterile defense against H5N1 HPAIV offered by the stable expression of chIFITM1 is inadequate; however, the clinical outcome can be substantially ameliorated. In conclusion, chIFITM proteins can inhibit influenza virus replication that can infect various host species and could be a crucial barrier against zoonotic infections.

ACS Style

Mohammed Rohaim; Mohammad Al-Natour; Mohammed Abdelsabour; Rania El Naggar; Yahia Madbouly; Kawkab Ahmed; Muhammad Munir. Transgenic Chicks Expressing Interferon-Inducible Transmembrane Protein 1 (IFITM1) Restrict Highly Pathogenic H5N1 Influenza Viruses. International Journal of Molecular Sciences 2021, 22, 8456 .

AMA Style

Mohammed Rohaim, Mohammad Al-Natour, Mohammed Abdelsabour, Rania El Naggar, Yahia Madbouly, Kawkab Ahmed, Muhammad Munir. Transgenic Chicks Expressing Interferon-Inducible Transmembrane Protein 1 (IFITM1) Restrict Highly Pathogenic H5N1 Influenza Viruses. International Journal of Molecular Sciences. 2021; 22 (16):8456.

Chicago/Turabian Style

Mohammed Rohaim; Mohammad Al-Natour; Mohammed Abdelsabour; Rania El Naggar; Yahia Madbouly; Kawkab Ahmed; Muhammad Munir. 2021. "Transgenic Chicks Expressing Interferon-Inducible Transmembrane Protein 1 (IFITM1) Restrict Highly Pathogenic H5N1 Influenza Viruses." International Journal of Molecular Sciences 22, no. 16: 8456.

Journal article
Published: 10 May 2021 in Comparative Immunology, Microbiology and Infectious Diseases
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Infectious bronchitis (IB) is a highly contagious viral disease and is responsible for considerable economic losses in the poultry industry, worldwide. To mitigate the IB-associated losses, multiple vaccines are being applied in the sector with variable successes and thus necessitating the development of a potent vaccine to protect against the IB in the poultry. In the present study, we investigated a bivalent live attenuated vaccine consisting of IB virus (IBV) strain H120 (GI-1 lineage) and D274 (GI-12 lineage) to evaluate its protection against heterologous variant of IBV (GI-23 lineage) in chicken. Protection efficacy was evaluated based on the serology, clinical signs, survival rates, tracheal and kidney histopathology and the viral shedding. Results demonstrated that administering live H120 and D274 (named here Classivar®) vaccine in one day-old and 14 days-old provided 100 % protection. We observed a significant increase in the mean antibody titers, reduced virus shedding, and ameliorated histopathology lesions compared to routinely used vaccination regimes. These results revealed that usage of different IBV vaccines combination can successfully ameliorate the clinical outcome and pathology in vaccinated chicks especially after booster vaccination regime using Classivar®. In conclusions, our data indicate that Classivar® vaccine is safe in chicks and may serve as an effective vaccine against the threat posed by commonly circulating IBV strains in the poultry industry.

ACS Style

Mohammad A. Abdel-Sabour; Mohammed A. Rohaim; Owais J.A. Salman; Samah E. Abodalal; Faten F. Mohammad; Mohammad S. Madkour; Nabil A. Abdel-Wanis; Muhammad Munir. Immunogenicity and efficacy of a bivalent vaccine against infectious bronchitis virus. Comparative Immunology, Microbiology and Infectious Diseases 2021, 77, 101670 .

AMA Style

Mohammad A. Abdel-Sabour, Mohammed A. Rohaim, Owais J.A. Salman, Samah E. Abodalal, Faten F. Mohammad, Mohammad S. Madkour, Nabil A. Abdel-Wanis, Muhammad Munir. Immunogenicity and efficacy of a bivalent vaccine against infectious bronchitis virus. Comparative Immunology, Microbiology and Infectious Diseases. 2021; 77 ():101670.

Chicago/Turabian Style

Mohammad A. Abdel-Sabour; Mohammed A. Rohaim; Owais J.A. Salman; Samah E. Abodalal; Faten F. Mohammad; Mohammad S. Madkour; Nabil A. Abdel-Wanis; Muhammad Munir. 2021. "Immunogenicity and efficacy of a bivalent vaccine against infectious bronchitis virus." Comparative Immunology, Microbiology and Infectious Diseases 77, no. : 101670.

Original article
Published: 19 April 2021 in Veterinary and Comparative Oncology
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Canine mammary carcinoma (CMC) is one of the major health threats in dogs. The oncolytic virotherapy is a promising strategy to treat canine as well as human cancer patients with non‐pathogenic replicating viruses. Here, we evaluated the antitumor activity of one lentogenic, non‐lytic Newcastle disease virus (NDV) LaSota strain expressing GFP (NDV‐GFP) on five different CMCs and one non‐tumorigenic cell line, regarding cell viability, cell death, selectivity index, morphology, global and target gene expression analysis. As evidenced by the selectivity index, all CMC cell lines were more susceptible to NDV‐GFP in comparison with the non‐tumorigenic cells (~3.1× to ~78.7×). In addition, the oncolytic effect of NDV‐GFP was more evident in more malignant CMC cells. Also, we observed an inverse association of the IFN pathway expression and the susceptibility to NDV. The downregulated genes in NDV‐GFP‐sensitive cells were functionally enriched for antiviral mechanisms by interferon and immune system pathways, demonstrating that these mechanisms are the most prominent for oncolysis by NDV. To our knowledge, this is the first description of oncolysis by an NDV strain in canine mammary cancer cells. We also demonstrated specific molecular pathways related to NDV susceptibility in these cancer cells, opening the possibility to use NDV as a therapeutic‐targeted option for more malignant CMCs. Therefore, these results urge for more studies using oncolytic NDVs, especially considering genetic editing to improve efficacy in dogs.

ACS Style

Mariana Rodrigues Santos; Pedro Luiz Porfírio Xavier; Pedro Ratto Lisboa Pires; Arina Lázaro Rochetti; Daniele Fernanda Rosim; Guilherme Pereira Scagion; Debora Aparecida Pires De Campos Zuccari; Muhammad Munir; Helena Lage Ferreira; Heidge Fukumasu. Oncolytic effect of Newcastle disease virus is attributed to interferon regulation in canine mammary cancer cell lines. Veterinary and Comparative Oncology 2021, 19, 593 -601.

AMA Style

Mariana Rodrigues Santos, Pedro Luiz Porfírio Xavier, Pedro Ratto Lisboa Pires, Arina Lázaro Rochetti, Daniele Fernanda Rosim, Guilherme Pereira Scagion, Debora Aparecida Pires De Campos Zuccari, Muhammad Munir, Helena Lage Ferreira, Heidge Fukumasu. Oncolytic effect of Newcastle disease virus is attributed to interferon regulation in canine mammary cancer cell lines. Veterinary and Comparative Oncology. 2021; 19 (3):593-601.

Chicago/Turabian Style

Mariana Rodrigues Santos; Pedro Luiz Porfírio Xavier; Pedro Ratto Lisboa Pires; Arina Lázaro Rochetti; Daniele Fernanda Rosim; Guilherme Pereira Scagion; Debora Aparecida Pires De Campos Zuccari; Muhammad Munir; Helena Lage Ferreira; Heidge Fukumasu. 2021. "Oncolytic effect of Newcastle disease virus is attributed to interferon regulation in canine mammary cancer cell lines." Veterinary and Comparative Oncology 19, no. 3: 593-601.

Journal article
Published: 25 February 2021 in Scientific Reports
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The addition of a methyl group to the N6-position of adenosine (m6A) is considered one of the most prevalent internal post-transcriptional modifications and is attributed to virus replication and cell biology. Viral epitranscriptome sequencing analysis has revealed that hemagglutinin (HA) mRNA of H1N1 carry eight m6A sites which are primarily enriched in 5′-DRACH-3′ sequence motif. Herein, a large-scale comparative m6A analysis was conducted to investigate the conservation patterns of the DRACH motifs that corresponding to the reference m6A sites among influenza A viruses. A total of 70,030 complete HA sequences that comprise all known HA subtypes (H1–18) collected over several years, countries, and affected host species were analysed on both mRNA and vRNA strands. The bioinformatic analysis revealed the highest degree of DRACHs conservation among all H1 sequences that clustered largely in the middle and in the vicinity to 3′ end with at least four DRACH motifs were conserved in all mRNA sequences. The major HA-containing subtypes displayed a modest DRACH motif conservation located either in the middle region of HA transcript (H3) or at the 3′ end (H5) or were distributed across the length of HA sequence (H9). The lowest conservation was demonstrated in HA subtypes that infect mostly the wild type avian species and bats. Interestingly, the total number and the conserved DRACH motifs in the vRNA were found to be much lower than those observed in the mRNA. Collectively, the identification of putative m6A topology provides a foundation for the future intervention of influenza infection, replication, and pathobiology in susceptible hosts.

ACS Style

Mahmoud Bayoumi; Muhammad Munir. Evolutionary conservation of the DRACH signatures of potential N6-methyladenosine (m6A) sites among influenza A viruses. Scientific Reports 2021, 11, 1 -12.

AMA Style

Mahmoud Bayoumi, Muhammad Munir. Evolutionary conservation of the DRACH signatures of potential N6-methyladenosine (m6A) sites among influenza A viruses. Scientific Reports. 2021; 11 (1):1-12.

Chicago/Turabian Style

Mahmoud Bayoumi; Muhammad Munir. 2021. "Evolutionary conservation of the DRACH signatures of potential N6-methyladenosine (m6A) sites among influenza A viruses." Scientific Reports 11, no. 1: 1-12.

Correction
Published: 30 January 2021 in Virus Genes
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The original version of this article unfortunately contained an error in figure.

ACS Style

Rania F. El Naggar; Mohammed A. Rohaim; Muhammad Munir. Correction to: Potential reverse spillover of infectious bursal disease virus at the interface of commercial poultry and wild birds. Virus Genes 2021, 57, 242 -244.

AMA Style

Rania F. El Naggar, Mohammed A. Rohaim, Muhammad Munir. Correction to: Potential reverse spillover of infectious bursal disease virus at the interface of commercial poultry and wild birds. Virus Genes. 2021; 57 (2):242-244.

Chicago/Turabian Style

Rania F. El Naggar; Mohammed A. Rohaim; Muhammad Munir. 2021. "Correction to: Potential reverse spillover of infectious bursal disease virus at the interface of commercial poultry and wild birds." Virus Genes 57, no. 2: 242-244.

Review
Published: 12 January 2021 in Frontiers in Cell and Developmental Biology
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The cellular RNA can acquire a variety of chemical modifications during the cell cycle, and compelling pieces of evidence highlight the importance of these modifications in determining the metabolism of RNA and, subsequently, cell physiology. Among myriads of modifications, methylation at the N6-position of adenosine (m6A) is the most important and abundant internal modification in the messenger RNA. The m6A marks are installed by methyltransferase complex proteins (writers) in the majority of eukaryotes and dynamically reversed by demethylases such as FTO and ALKBH5 (erasers). The incorporated m6A marks on the RNA transcripts are recognized by m6A-binding proteins collectively called readers. Recent epigenetic studies have unequivocally highlighted the association of m6A demethylases with a range of biomedical aspects, including human diseases, cancers, and metabolic disorders. Moreover, the mechanisms of demethylation by m6A erasers represent a new frontier in the future basic research on RNA biology. In this review, we focused on recent advances describing various physiological, pathological, and viral regulatory roles of m6A erasers. Additionally, we aim to analyze structural insights into well-known m6A-demethylases in assessing their substrate binding-specificity, efficiency, and selectivity. Knowledge on cellular and viral RNA metabolism will shed light on m6A-specific recognition by demethylases and will provide foundations for the future development of efficacious therapeutic agents to various cancerous conditions and open new avenues for the development of antivirals.

ACS Style

Mahmoud Bayoumi; Muhammad Munir. Structural Insights Into m6A-Erasers: A Step Toward Understanding Molecule Specificity and Potential Antiviral Targeting. Frontiers in Cell and Developmental Biology 2021, 8, 1 .

AMA Style

Mahmoud Bayoumi, Muhammad Munir. Structural Insights Into m6A-Erasers: A Step Toward Understanding Molecule Specificity and Potential Antiviral Targeting. Frontiers in Cell and Developmental Biology. 2021; 8 ():1.

Chicago/Turabian Style

Mahmoud Bayoumi; Muhammad Munir. 2021. "Structural Insights Into m6A-Erasers: A Step Toward Understanding Molecule Specificity and Potential Antiviral Targeting." Frontiers in Cell and Developmental Biology 8, no. : 1.

Preprint content
Published: 11 January 2021
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The global deployment of an effective and safe vaccine is currently a public health priority to curtail the coronavirus disease 2019 (COVID-19) pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Here, we evaluated a Newcastle disease virus (NDV)-based intranasal vectored-vaccine in mice and hamsters for its immunogenicity, safety and protective efficacy in challenge studies with SARS-CoV-2. The recombinant (r)NDV-S vaccine expressing spike (S) protein of SARS-CoV-2 administrated via intranasal route in mice induced high levels of SARS-CoV-2-specific neutralizing immunoglobulin A (IgA) and IgG2a antibodies and T cell-mediated immunity. Hamsters vaccinated with two doses of vaccine showed complete protection from clinical disease including lung infection, inflammation, and pathological lesions after SARS-CoV-2 challenge. Importantly, a single or double dose of intranasal rNDV-S vaccine completely blocked SARS-CoV-2 shedding in nasal turbinate and lungs within 4 days of vaccine administration in hamsters. Taken together, intranasal administration of rNDV-S has the potential to control infection at the site of inoculation, which should prevent both the clinical disease and transmission to halt the spread of the COVID-19 pandemic.

ACS Style

Jun-Guy Park; Fatai S. Oladunni; Mohammed A. Rohaim; Jayde Whittingham-Dowd; James Tollitt; Bakri M Assas; Wafaa Alhazmi; Abdullah Almilaibary; Munir Iqbal; Pengxiang Chang; Renee Escalona; Vinay Shivanna; Jordi B. Torrelles; John J Worthington; Lucy H. Jackson-Jones; Luis Martinez-Sobrido; Muhammad Munir. Immunogenicity and Protective Efficacy of an Intranasal Live-attenuated Vaccine Against SARS-CoV-2 in Preclinical Animal Models. 2021, 1 .

AMA Style

Jun-Guy Park, Fatai S. Oladunni, Mohammed A. Rohaim, Jayde Whittingham-Dowd, James Tollitt, Bakri M Assas, Wafaa Alhazmi, Abdullah Almilaibary, Munir Iqbal, Pengxiang Chang, Renee Escalona, Vinay Shivanna, Jordi B. Torrelles, John J Worthington, Lucy H. Jackson-Jones, Luis Martinez-Sobrido, Muhammad Munir. Immunogenicity and Protective Efficacy of an Intranasal Live-attenuated Vaccine Against SARS-CoV-2 in Preclinical Animal Models. . 2021; ():1.

Chicago/Turabian Style

Jun-Guy Park; Fatai S. Oladunni; Mohammed A. Rohaim; Jayde Whittingham-Dowd; James Tollitt; Bakri M Assas; Wafaa Alhazmi; Abdullah Almilaibary; Munir Iqbal; Pengxiang Chang; Renee Escalona; Vinay Shivanna; Jordi B. Torrelles; John J Worthington; Lucy H. Jackson-Jones; Luis Martinez-Sobrido; Muhammad Munir. 2021. "Immunogenicity and Protective Efficacy of an Intranasal Live-attenuated Vaccine Against SARS-CoV-2 in Preclinical Animal Models." , no. : 1.

Review article
Published: 11 December 2020 in Frontiers in Cellular and Infection Microbiology
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Interferons are an essential component of the innate arm of the immune system and are arguably one of the most important lines of defence against viruses. The human IFN system and its functionality has already been largely characterized and studied in detail. However, the IFN systems of bats have only been marginally examined to date up until the recent developments of the Bat1k project which have now opened new opportunities in research by identifying six new bat genomes to possess novel genes that are likely associated with viral tolerance exhibited in bats. Interestingly, bats have been hypothesized to possess the ability to establish a host-virus relationship where despite being infected, they exhibit limited signs of disease and still retain the ability to transmit the disease into other susceptible hosts. Bats are one of the most abundant and widespread vertebrates on the planet and host many zoonotic viruses that are highly pathogenic to humans. Several genomics, immunological, and biological features are thought to underlie novel antiviral mechanisms of bats. This review aims to explore the bat IFN system and developments in its diverse IFN features, focusing mainly on the model species, the Australian black flying fox (Pteropus alecto), while also highlighting bat innate immunity as an exciting and fruitful area of research to understand their ability to control viral-mediated pathogenesis.

ACS Style

Emily Clayton; Muhammad Munir. Fundamental Characteristics of Bat Interferon Systems. Frontiers in Cellular and Infection Microbiology 2020, 10, 527921 .

AMA Style

Emily Clayton, Muhammad Munir. Fundamental Characteristics of Bat Interferon Systems. Frontiers in Cellular and Infection Microbiology. 2020; 10 ():527921.

Chicago/Turabian Style

Emily Clayton; Muhammad Munir. 2020. "Fundamental Characteristics of Bat Interferon Systems." Frontiers in Cellular and Infection Microbiology 10, no. : 527921.

Author correction
Published: 27 November 2020 in Scientific Reports
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An amendment to this paper has been published and can be accessed via a link at the top of the paper.

ACS Style

Muhammad Zubair Shabbir; Aziz-Ul Rahman; Muhammad Munir. Author Correction: A comprehensive global perspective on phylogenomics and evolutionary dynamics of Small ruminant morbillivirus. Scientific Reports 2020, 10, 1 -3.

AMA Style

Muhammad Zubair Shabbir, Aziz-Ul Rahman, Muhammad Munir. Author Correction: A comprehensive global perspective on phylogenomics and evolutionary dynamics of Small ruminant morbillivirus. Scientific Reports. 2020; 10 (1):1-3.

Chicago/Turabian Style

Muhammad Zubair Shabbir; Aziz-Ul Rahman; Muhammad Munir. 2020. "Author Correction: A comprehensive global perspective on phylogenomics and evolutionary dynamics of Small ruminant morbillivirus." Scientific Reports 10, no. 1: 1-3.

Review
Published: 24 November 2020 in Frontiers in Cellular and Infection Microbiology
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Clustered regularly interspaced short palindromic repeats associated protein nuclease 9 (CRISPR-Cas9) technology offers novel approaches to precisely, cost-effectively, and user-friendly edit genomes for a wide array of applications and across multiple disciplines. This methodology can be leveraged to underpin host-virus interactions, elucidate viral gene functions, and to develop recombinant vaccines. The successful utilization of CRISPR/Cas9 in editing viral genomes has paved the way of developing novel and multiplex viral vectored poultry vaccines. Furthermore, CRISPR/Cas9 can be exploited to rectify major limitations of conventional approaches including reversion to virulent form, recombination with field viruses and transgene, and genome instability. This review provides comprehensive analysis of the potential of CRISPR/Cas9 genome editing technique in understanding avian virus-host interactions and developing novel poultry vaccines. Finally, we discuss the simplest and practical aspects of genome editing approaches in generating multivalent recombinant poultry vaccines that conform simultaneous protection against major avian diseases.

ACS Style

Julianne Vilela; Mohammed A. Rohaim; Muhammad Munir. Application of CRISPR/Cas9 in Understanding Avian Viruses and Developing Poultry Vaccines. Frontiers in Cellular and Infection Microbiology 2020, 10, 1 .

AMA Style

Julianne Vilela, Mohammed A. Rohaim, Muhammad Munir. Application of CRISPR/Cas9 in Understanding Avian Viruses and Developing Poultry Vaccines. Frontiers in Cellular and Infection Microbiology. 2020; 10 ():1.

Chicago/Turabian Style

Julianne Vilela; Mohammed A. Rohaim; Muhammad Munir. 2020. "Application of CRISPR/Cas9 in Understanding Avian Viruses and Developing Poultry Vaccines." Frontiers in Cellular and Infection Microbiology 10, no. : 1.

Review article
Published: 23 November 2020 in Microbial Pathogenesis
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Coronaviruses (CoVs) are causing a number of human and animal diseases because of their zoonotic nature such as Middle East respiratory syndrome (MERS), severe acute respiratory syndrome (SARS) and coronavirus disease 2019 (COVID-19). These viruses can infect respiratory, gastrointestinal, hepatic and central nervous systems of human, livestock, birds, bat, mouse, and many wild animals. The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a newly emerging respiratory virus and is causing CoVID-19 with high morbidity and considerable mortality. All CoVs belong to the order Nidovirales, family Coronaviridae, are enveloped positive-sense RNA viruses, characterised by club-like spikes on their surfaces and large RNA genome with a distinctive replication strategy. Coronavirus have the largest RNA genomes (∼26–32 kilobases) and their expansion was likely enabled by acquiring enzyme functions that counter the commonly high error frequency of viral RNA polymerases. Non-structural proteins (nsp) 7–16 are cleaved from two large replicase polyproteins and guide the replication and processing of coronavirus RNA. Coronavirus replicase has more or less universal activities, such as RNA polymerase (nsp 12) and helicase (nsp 13), as well as a variety of unusual or even special mRNA capping (nsp 14, nsp 16) and fidelity regulation (nsp 14) domains. Besides that, several smaller subunits (nsp 7– nsp 10) serve as essential cofactors for these enzymes and contribute to the emerging “nsp interactome.” In spite of the significant progress in studying coronaviruses structural and functional properties, there is an urgent need to understand the coronaviruses evolutionary success that will be helpful to develop enhanced control strategies. Therefore, it is crucial to understand the structure, function, and interactions of coronaviruses RNA synthesizing machinery and their replication strategies.

ACS Style

Mohammed A. Rohaim; Rania F. El Naggar; Emily Clayton; Muhammad Munir. Structural and functional insights into non-structural proteins of coronaviruses. Microbial Pathogenesis 2020, 150, 104641 -104641.

AMA Style

Mohammed A. Rohaim, Rania F. El Naggar, Emily Clayton, Muhammad Munir. Structural and functional insights into non-structural proteins of coronaviruses. Microbial Pathogenesis. 2020; 150 ():104641-104641.

Chicago/Turabian Style

Mohammed A. Rohaim; Rania F. El Naggar; Emily Clayton; Muhammad Munir. 2020. "Structural and functional insights into non-structural proteins of coronaviruses." Microbial Pathogenesis 150, no. : 104641-104641.

Journal article
Published: 19 November 2020 in Comparative Immunology, Microbiology and Infectious Diseases
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Despite the recent advances in avian influenza virus surveillance and genomic data, fundamental questions concerning the ecology and evolution of these viruses remain elusive. In Egypt, the H5N8 highly pathogenic avian influenza viruses (HPAIVs) are co-circulating simultaneously with HPAIVs of subtypes H5N1 and low-pathogenic avian influenza viruses (LPAIVs) of subtype H9N2 in both commercial and backyard poultry. In order to isolate AIV from wild birds and to assess their potential in causing infection in commercial poultry, a total of thirty-four cloacal swab samples were collected from apparently healthy migratory wild birds (Anas acuta, Anas crecca, Rallus aquaticus, and Bubulcus ibis) from four Egyptian Governorates (Giza, Menoufia, Gharbia, and Dakahlia). Based on matrix (M) gene-targeting real-time reverse transcriptase PCR and subsequent genetic characterization, our results revealed two positive isolates (2/34) for H5N8 whereas no H5N1 and H9N2 subtypes were detected. Genetic characterization of the full-length haemagglutinin (HA) genes revealed the clustering of two reported isolates within group B of clade 2.3.4.4. The potential of a wild bird-origin H5N8 virus isolated from a cattle egret for its transmission capability within and between chickens was investigated in compare to chicken origin H5N8 AIV. Chickens inoculated with cattle egret isolate showed varying clinical signs and detection of virus shedding. In contrast, the contact chickens showed less levels of virus secretion indicating efficient virus inter/intra-species transmission. These results demonstrated the possibility of spread of wild bird origin H5N8 viruses between chicken. In conclusion, our study highlights the need for continuous and frequent monitoring of the genetic diversity of H5N8 AIVs in wild birds as well as commercial poultry sectors for better understanding and determining the genetic nature of these viruses, which is fundamental to predict any future threat through virus reassortment with the potential to threaten human and animal health. Likewise, an assessment of coverage and efficacy of different vaccines and or vaccination regimes in the field conditions should be reconsidered along with strict biosecurity measures.

ACS Style

Mohammed A. Rohaim; Rania F. El Naggar; Yehia Madbouly; Mohammed A. AbdelSabour; Kawkab A. Ahmed; Muhammad Munir. Comparative infectivity and transmissibility studies of wild-bird and chicken-origin highly pathogenic avian influenza viruses H5N8 in chickens. Comparative Immunology, Microbiology and Infectious Diseases 2020, 74, 101594 .

AMA Style

Mohammed A. Rohaim, Rania F. El Naggar, Yehia Madbouly, Mohammed A. AbdelSabour, Kawkab A. Ahmed, Muhammad Munir. Comparative infectivity and transmissibility studies of wild-bird and chicken-origin highly pathogenic avian influenza viruses H5N8 in chickens. Comparative Immunology, Microbiology and Infectious Diseases. 2020; 74 ():101594.

Chicago/Turabian Style

Mohammed A. Rohaim; Rania F. El Naggar; Yehia Madbouly; Mohammed A. AbdelSabour; Kawkab A. Ahmed; Muhammad Munir. 2020. "Comparative infectivity and transmissibility studies of wild-bird and chicken-origin highly pathogenic avian influenza viruses H5N8 in chickens." Comparative Immunology, Microbiology and Infectious Diseases 74, no. : 101594.

Original paper
Published: 24 September 2020 in Virus Genes
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Recently, multiple spillover events between domesticated poultry and wild birds have been reported for several avian viruses. This phenomenon highlights the importance of the livestock-wildlife interface in the possible emergence of novel viruses. The aim of the current study was to investigate the potential spillover and epidemiological links of infectious bursal disease virus (IBDV) between wild birds and domestic poultry. To this end, twenty-eight cloacal swabs were collected from four species of free-living Egyptian wild birds (i.e. mallard duck, bean goose, white-fronted goose and black-billed magpie). Genetic and phylogenetic analysis of three positive isolates revealed that the IBDV/USC-1/2019 strain clustered with previously reported very virulent IBDV (vvIBDV) Egyptian isolates. Interestingly, two other wild bird-origin isolates (i.e. IBDV/USC-2/2019 and IBDV/USC-3/2019) grouped with a vaccine strain that is being used in commercial poultry. In conclusion, our results revealed the molecular detection of vaccine and vvIBDV-like strains in Egyptian wild birds and highlighted the potential role of wild birds in IBDV epidemiology in disease-endemic regions.

ACS Style

Rania F. El Naggar; Mohammed A. Rohaim; Muhammad Munir. Potential reverse spillover of infectious bursal disease virus at the interface of commercial poultry and wild birds. Virus Genes 2020, 56, 705 -711.

AMA Style

Rania F. El Naggar, Mohammed A. Rohaim, Muhammad Munir. Potential reverse spillover of infectious bursal disease virus at the interface of commercial poultry and wild birds. Virus Genes. 2020; 56 (6):705-711.

Chicago/Turabian Style

Rania F. El Naggar; Mohammed A. Rohaim; Muhammad Munir. 2020. "Potential reverse spillover of infectious bursal disease virus at the interface of commercial poultry and wild birds." Virus Genes 56, no. 6: 705-711.

Journal article
Published: 01 September 2020 in Viruses
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Until vaccines and effective therapeutics become available, the practical solution to transit safely out of the current coronavirus disease 19 (CoVID-19) lockdown may include the implementation of an effective testing, tracing and tracking system. However, this requires a reliable and clinically validated diagnostic platform for the sensitive and specific identification of SARS-CoV-2. Here, we report on the development of a de novo, high-resolution and comparative genomics guided reverse-transcribed loop-mediated isothermal amplification (LAMP) assay. To further enhance the assay performance and to remove any subjectivity associated with operator interpretation of results, we engineered a novel hand-held smart diagnostic device. The robust diagnostic device was further furnished with automated image acquisition and processing algorithms and the collated data was processed through artificial intelligence (AI) pipelines to further reduce the assay run time and the subjectivity of the colorimetric LAMP detection. This advanced AI algorithm-implemented LAMP (ai-LAMP) assay, targeting the RNA-dependent RNA polymerase gene, showed high analytical sensitivity and specificity for SARS-CoV-2. A total of ~200 coronavirus disease (CoVID-19)-suspected NHS patient samples were tested using the platform and it was shown to be reliable, highly specific and significantly more sensitive than the current gold standard qRT-PCR. Therefore, this system could provide an efficient and cost-effective platform to detect SARS-CoV-2 in resource-limited laboratories.

ACS Style

Mohammed Rohaim; Emily Clayton; Irem Sahin; Julianne Vilela; Manar Khalifa; Mohammad Al-Natour; Mahmoud Bayoumi; Aurore Poirier; Manoharanehru Branavan; Mukunthan Tharmakulasingam; Nouman Chaudhry; Ravinder Sodi; Amy Brown; Peter Burkhart; Wendy Hacking; Judy Botham; Joe Boyce; Hayley Wilkinson; Craig Williams; Jayde Whittingham-Dowd; Elisabeth Shaw; Matt Hodges; Lisa Butler; Michelle Bates; Roberto La Ragione; Wamadeva Balachandran; Anil Fernando; Muhammad Munir. Artificial Intelligence-Assisted Loop Mediated Isothermal Amplification (ai-LAMP) for Rapid Detection of SARS-CoV-2. Viruses 2020, 12, 972 .

AMA Style

Mohammed Rohaim, Emily Clayton, Irem Sahin, Julianne Vilela, Manar Khalifa, Mohammad Al-Natour, Mahmoud Bayoumi, Aurore Poirier, Manoharanehru Branavan, Mukunthan Tharmakulasingam, Nouman Chaudhry, Ravinder Sodi, Amy Brown, Peter Burkhart, Wendy Hacking, Judy Botham, Joe Boyce, Hayley Wilkinson, Craig Williams, Jayde Whittingham-Dowd, Elisabeth Shaw, Matt Hodges, Lisa Butler, Michelle Bates, Roberto La Ragione, Wamadeva Balachandran, Anil Fernando, Muhammad Munir. Artificial Intelligence-Assisted Loop Mediated Isothermal Amplification (ai-LAMP) for Rapid Detection of SARS-CoV-2. Viruses. 2020; 12 (9):972.

Chicago/Turabian Style

Mohammed Rohaim; Emily Clayton; Irem Sahin; Julianne Vilela; Manar Khalifa; Mohammad Al-Natour; Mahmoud Bayoumi; Aurore Poirier; Manoharanehru Branavan; Mukunthan Tharmakulasingam; Nouman Chaudhry; Ravinder Sodi; Amy Brown; Peter Burkhart; Wendy Hacking; Judy Botham; Joe Boyce; Hayley Wilkinson; Craig Williams; Jayde Whittingham-Dowd; Elisabeth Shaw; Matt Hodges; Lisa Butler; Michelle Bates; Roberto La Ragione; Wamadeva Balachandran; Anil Fernando; Muhammad Munir. 2020. "Artificial Intelligence-Assisted Loop Mediated Isothermal Amplification (ai-LAMP) for Rapid Detection of SARS-CoV-2." Viruses 12, no. 9: 972.

Journal article
Published: 24 August 2020 in Vaccines
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The severe acute respiratory syndrome-coronavirus 2 (SARS-CoV-2) caused an ongoing unprecedented global public health crises of coronavirus disease in 2019 (CoVID-19). The precipitously increased death rates, its impact on livelihood and trembling economies warrant the urgent development of a SARS-CoV-2 vaccine which would be safe, efficacious and scalable. Owing to unavailability of the vaccine, we propose a de novo synthesized avian orthoavulavirus 1 (AOaV-1)-based topical respiratory vaccine candidate against CoVID-19. Avirulent strain of AOaV-1 was engineered to express full length spike (S) glycoprotein which is highly neutralizing and a major protective antigen of the SARS-CoV-2. Broad-scale in vitro characterization of a recombinant vaccine candidate demonstrated efficient co-expression of the hemagglutinin-neuraminidase (HN) of AOaV-1 and S protein of SARS-CoV-2, and comparable replication kinetics were observed in a cell culture model. The recombinant vaccine candidate virus actively replicated and spread within cells independently of exogenous trypsin. Interestingly, incorporation of S protein of SARS-CoV-2 into the recombinant AOaV-1 particles attributed the sensitivity to anti-SARS-CoV-2 antiserum and more prominently to anti-AOaV-1 antiserum. Finally, our results demonstrated that the recombinant vaccine vector stably expressed S protein after multiple propagations in chicken embryonated eggs, and this expression did not significantly impact the in vitro growth characteristics of the recombinant. Taken together, the presented respiratory vaccine candidate is highly attenuated in primates per se, safe and lacking pre-existing immunity in human, and carries the potential for accelerated vaccine development against CoVID-19 for clinical studies.

ACS Style

Mohammed Rohaim; Muhammad Munir. A Scalable Topical Vectored Vaccine Candidate against SARS-CoV-2. Vaccines 2020, 8, 472 .

AMA Style

Mohammed Rohaim, Muhammad Munir. A Scalable Topical Vectored Vaccine Candidate against SARS-CoV-2. Vaccines. 2020; 8 (3):472.

Chicago/Turabian Style

Mohammed Rohaim; Muhammad Munir. 2020. "A Scalable Topical Vectored Vaccine Candidate against SARS-CoV-2." Vaccines 8, no. 3: 472.

Original research article
Published: 15 July 2020 in Frontiers in Cell and Developmental Biology
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The addition of a methyl group to the N6 position of adenosine (m6A) is the most common posttranscriptional RNA modification, and it regulates most steps of RNA metabolism including splicing, stability, translation, nuclear-export, and RNA structures. Besides cellular RNA, m6A modifications have also been detected on viral RNA. A range of recent studies have demonstrated the crucial roles of m6A in the virus–host interactions; however, m6A cellular machineries are only characterized in limited mammalian species. Herein, we aim to present comprehensive evolutionary insights into major m6A writers, erasers, and readers and draw a comparative structural analysis between avian and mammalian m6A-associated machineries. The comparative collinearity on the chromosomal scale revealed that the majority of m6A-related genes were found less syntenic even among avian species. Genetic analysis of avian m6A erasers revealed a distinct phylogenetic clustering compared to mammalian orthologs and shared a weak percent (55%) identity with mammalian species with low identity percentage (55%). The overall comparative three-dimensional (3D) structure analyses among different mammalian species were maintained through synonymous structural mutations. Unlike erasers, the putative 3D structures in the active sites as for the aromatic cage in YTH-domain of YTHDC1 and two pivotal loops in MTD-domains in METTL3 exhibited structural alterations in chicken. In conjunction with in silico investigations, influenza viruses significantly downregulated gene the transcription of m6A writers and erasers, whereas m6A readers were moderately regulated in chicken fibroblasts. In light of these findings, future detailed biochemical and crystallographic studies are warranted to define the roles of m6A machinery in regulating both viral and cellular RNA metabolism in avian species.

ACS Style

Mahmoud Bayoumi; Mohammed Abdelmohsen Shahaat Rohaim; Muhammad Munir. Structural and Virus Regulatory Insights Into Avian N6-Methyladenosine (m6A) Machinery. Frontiers in Cell and Developmental Biology 2020, 8, 543 .

AMA Style

Mahmoud Bayoumi, Mohammed Abdelmohsen Shahaat Rohaim, Muhammad Munir. Structural and Virus Regulatory Insights Into Avian N6-Methyladenosine (m6A) Machinery. Frontiers in Cell and Developmental Biology. 2020; 8 ():543.

Chicago/Turabian Style

Mahmoud Bayoumi; Mohammed Abdelmohsen Shahaat Rohaim; Muhammad Munir. 2020. "Structural and Virus Regulatory Insights Into Avian N6-Methyladenosine (m6A) Machinery." Frontiers in Cell and Developmental Biology 8, no. : 543.

Other
Published: 10 July 2020
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Until vaccines and effective therapeutics become available, the practical way to transit safely out of the current lockdown may include the implementation of an effective testing, tracing and tracking system. However, this requires a reliable and clinically validated diagnostic platform for the sensitive and specific identification of SARS-CoV-2. Here, we report on the development of a de novo, high-resolution and comparative genomics guided reverse-transcribed loop-mediated isothermal amplification (LAMP) assay. To further enhance the assay performance and to remove any subjectivity associated with operator interpretation of result, we engineered a novel hand-held smart diagnostic device. The robust diagnostic device was further furnished with automated image acquisition and processing algorithms, and the collated data was processed through artificial intelligence (AI) pipelines to further reduce the assay run time and the subjectivity of the colorimetric LAMP detection. This advanced AI algorithm-implemented LAMP (ai-LAMP) assay, targeting the RNA-dependent RNA polymerase gene, showed high analytical sensitivity and specificity for SARS-CoV-2. A total of ∼200 coronavirus disease (CoVID-19)-suspected patient samples were tested using the platform and it was shown to be reliable, highly specific and significantly more sensitive than the current gold standard qRT-PCR. The system could provide an efficient and cost-effective platform to detect SARS-CoV-2 in resource-limited laboratories.

ACS Style

Mohammed A Rohaim; Emily Clayton; Irem Sahin; Julianne Vilela; Manar E Khalifa; Mohammed Q Al-Natour; Mahmoud Bayoumi; Aurore Poirier; Manoharanehru Branavan; Mukunthan Tharmakulasingam; Nouman S Chaudhry; Ravinder Sodi; Amy Brown; Peter Burkhart; Wendy Hacking; Judy Botham; Joe Boyce; Hayley Wilkinson; Craig Williams; Michelle Bates; Roberto La Ragione; Wamadeva Balachandran; Anil Fernando; Muhammad Munir. Artificial Intelligence-Assisted Loop Mediated Isothermal Amplification (ai-LAMP) for Rapid and Reliable Detection of SARS-CoV-2. 2020, 1 .

AMA Style

Mohammed A Rohaim, Emily Clayton, Irem Sahin, Julianne Vilela, Manar E Khalifa, Mohammed Q Al-Natour, Mahmoud Bayoumi, Aurore Poirier, Manoharanehru Branavan, Mukunthan Tharmakulasingam, Nouman S Chaudhry, Ravinder Sodi, Amy Brown, Peter Burkhart, Wendy Hacking, Judy Botham, Joe Boyce, Hayley Wilkinson, Craig Williams, Michelle Bates, Roberto La Ragione, Wamadeva Balachandran, Anil Fernando, Muhammad Munir. Artificial Intelligence-Assisted Loop Mediated Isothermal Amplification (ai-LAMP) for Rapid and Reliable Detection of SARS-CoV-2. . 2020; ():1.

Chicago/Turabian Style

Mohammed A Rohaim; Emily Clayton; Irem Sahin; Julianne Vilela; Manar E Khalifa; Mohammed Q Al-Natour; Mahmoud Bayoumi; Aurore Poirier; Manoharanehru Branavan; Mukunthan Tharmakulasingam; Nouman S Chaudhry; Ravinder Sodi; Amy Brown; Peter Burkhart; Wendy Hacking; Judy Botham; Joe Boyce; Hayley Wilkinson; Craig Williams; Michelle Bates; Roberto La Ragione; Wamadeva Balachandran; Anil Fernando; Muhammad Munir. 2020. "Artificial Intelligence-Assisted Loop Mediated Isothermal Amplification (ai-LAMP) for Rapid and Reliable Detection of SARS-CoV-2." , no. : 1.

Preprint content
Published: 01 June 2020
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The severe acute respiratory syndrome-coronavirus 2 (SARS-CoV-2) caused an ongoing unprecedented global public health crises of coronavirus disease in 2019 (CoVID-19). The precipitously increased death rates, its impact on livelihood and trembling economies warrant the urgent development of SARS-CoV-2 vaccine which would be safe, efficacious and scalable. Owing to unavailability of the vaccine, we propose a de novo synthesised avian orthoavulavirus 1 (AOaV-1)-based topical respiratory vaccine candidate against CoVID-19. Avirulent strain of Newcastle disease virus, proto-type virus of AOaV-1, was engineered to express full length spike (S) glycoprotein which is highly neutralizing and major protective antigen of the SARS-CoV-2. Broad-scale in vitro characterization of recombinant vaccine candidate demonstrated efficient co-expression of the hemagglutinin-neuraminidase (HN) of AOaV-1 and S protein of SARS-CoV-2, and comparable replication kinetics were observed in cell culture model. The recombinant vaccine candidate virus actively replicated and spread within cells independently of exogenous trypsin. Interestingly, incorporation of S protein of SARS-CoV-2 into the recombinant AOaV-1 particles attributed the sensitivity to anti-SARS-CoV-2 antiserum and more prominently to anti-AOaV-1 antiserum. Finally, our results demonstrated that the recombinant vaccine vector stably expressed S protein after multiple propagation in chicken embryonated eggs, and this expression did not significantly impact the in vitro growth characteristics of the recombinant. Taken together, the presented respiratory vaccine candidate is highly attenuated in primates per se, safe and lacking pre-existing immunity in human, and carries the potential for accelerated vaccine development against CoVID-19 for clinical studies.

ACS Style

Mohammed A Rohaim; Muhammad Munir. A Scalable Topical Vectored Vaccine Candidate Against SARS-CoV-2. 2020, 1 .

AMA Style

Mohammed A Rohaim, Muhammad Munir. A Scalable Topical Vectored Vaccine Candidate Against SARS-CoV-2. . 2020; ():1.

Chicago/Turabian Style

Mohammed A Rohaim; Muhammad Munir. 2020. "A Scalable Topical Vectored Vaccine Candidate Against SARS-CoV-2." , no. : 1.

Journal article
Published: 29 May 2020 in Genes
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In the last 5 years, frequent outbreaks of infectious bronchitis virus (IBV) are observed in both broiler and layer chicken flocks in the Kingdom of Saudi Arabia (KSA) in spite of extensive usage of vaccines. The IBV is a widespread avian coronavirus affecting both vaccinated and unvaccinated chicken flocks and is attributed to significant economic losses, around the globe. In the present study, 58 (n = 58) samples were collected from four different commercial poultry flocks from 8 KSA districts during 2019. A total of nine positive isolates (9/58; 15.5%), based on real-time reverse transcriptase PCR targeting nucleocapsid (N) gene, were used for further genetic characterization and evolutionary analysis. Genetic characterization of the partial spike (S1) gene revealed the clustering of the reported isolates into three different genotypes, whereas four additional isolates were grouped within 4/91 genotype, two isolates within IS/885 genotype, one isolate was closely related to IS/1494/06, and two isolates were grouped within classic serotype (vaccine-like strains). Phylodynamic revealed clustering of four isolated viruses within GI-13 lineage, three isolates within GI-23 lineage, and two isolates within GI-1 lineage. Results indicate that there are high evolutionary distances between the newly identified IBV strains in this study and the commercially used vaccines (GI-1), suggesting that IBV strains circulating in the KSA are under constant evolutionary pressures. Selective pressure biostatistics analyses consistently demonstrate the presence of a higher positive score which highlights the role of natural selection, a mechanism of virus evolution on sites located on the protein surface, within or nearby domains involved in viral attachment or related functions. Recombination analysis revealed emergence of two isolates through recombination events resulting in new recombinant viruses. Taken together, these finding demonstrate the genetic and evolutionary insights into the currently circulating IBV genotypes in KSA, which could help to better understand the origin, spread, and evolution of infectious bronchitis viruses, and to ascertain the importance of disease monitoring as well as re-evaluation for the currently used vaccines and vaccination programs.

ACS Style

Mohammed A. Rohaim; Rania F. El El Naggar; Mohammed A. Abdelsabour; Mahmoud H. A. Mohamed; Ibrahim M. El-Sabagh; Muhammad Munir. Evolutionary Analysis of Infectious Bronchitis Virus Reveals Marked Genetic Diversity and Recombination Events. Genes 2020, 11, 1 .

AMA Style

Mohammed A. Rohaim, Rania F. El El Naggar, Mohammed A. Abdelsabour, Mahmoud H. A. Mohamed, Ibrahim M. El-Sabagh, Muhammad Munir. Evolutionary Analysis of Infectious Bronchitis Virus Reveals Marked Genetic Diversity and Recombination Events. Genes. 2020; 11 (6):1.

Chicago/Turabian Style

Mohammed A. Rohaim; Rania F. El El Naggar; Mohammed A. Abdelsabour; Mahmoud H. A. Mohamed; Ibrahim M. El-Sabagh; Muhammad Munir. 2020. "Evolutionary Analysis of Infectious Bronchitis Virus Reveals Marked Genetic Diversity and Recombination Events." Genes 11, no. 6: 1.