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Vesicular Stomatitis Virus Chimeras Expressing the Oropouche Virus Glycoproteins Elicit bioRxiv preprint doi: https://doi.org/10.1101/2021.02.19.432025; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Vesicular stomatitis virus chimeras expressing the Oropouche virus glycoproteins elicit 2 protective immune responses in mice. 3 4 Sarah Hulsey Stubbs1, Marjorie Cornejo Pontelli2, Nischay Mishra3, Changhong Zhou1, Juliano 5 de Paula Souza4, Rosa Maria Mendes Viana4, W. Ian Lipkin3, David M. Knipe1, Eurico Arruda4, 6 Sean P. J. Whelan2* 7 8 9 10 1Department of Microbiology, Harvard Medical School, Boston, Massachusetts, USA 11 2Department of Molecular Microbiology, Washington University School of Medicine in St. Louis, 12 Saint Louis, Missouri, USA 13 3Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New 14 York, New York, USA 15 4Department of Cell and Molecular Biology, Virology Research Center, Ribeirao Preto School of 16 Medicine, University of São Paulo, Ribeirao Preto, São Paulo, Brazil 17 18 *correspondence [email protected] 19 20 21 22 23 24 25 26 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.19.432025; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 27 Importance 28 Oropouche virus (OROV), an orthobunyavirus found in Central and South America, is an 29 emerging public health challenge that causes debilitating febrile illness. OROV is transmitted by 30 arthropods, and increasing mobilization has the potential to significantly increase the spread of 31 OROV globally. Despite this, no therapeutics or vaccines have been developed to combat 32 infection. Using vesicular stomatitis (VSV) as a backbone, we developed a chimeric virus 33 bearing the OROV glycoproteins (VSV-OROV) and tested its ability to elicit a neutralizing 34 antibody response. Our results demonstrate that VSV-OROV produces a strong neutralizing 35 antibody response that is at least partially targeted to the N-terminal region of Gc. Importantly, 36 vaccination with VSV-OROV reduces viral loads in mice challenged with wildtype virus. This 37 data provides the first evidence that targeting the OROV glycoproteins may be an effective 38 vaccination strategy to combat OROV infection. bioRxiv preprint doi: https://doi.org/10.1101/2021.02.19.432025; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 39 Abstract 40 Oropouche virus (OROV) infection of humans is associated with a debilitating febrile 41 illness that can progress to meningitis or encephalitis. First isolated from a forest worker in 42 Trinidad and Tobago in 1955, the arbovirus OROV has since been detected throughout the 43 Amazon basin with an estimated 500,000 human infections. Like other members of the family 44 Peribunyaviridae, the viral genome exists as 3 single-stranded negative-sense RNA segments. 45 The medium sized segment encodes a viral glycoprotein complex (GPC) that is proteolytically 46 processed into two viral envelope proteins Gn and Gc responsible for attachment and membrane 47 fusion. There are no therapeutics or vaccines to combat OROV infection, and we have little 48 understanding of protective immunity to infection. Here we generated a replication competent 49 chimeric vesicular stomatitis virus (VSV), in which the endogenous glycoprotein was replaced by 50 the GPC of OROV. Serum from mice immunized with VSV-OROV specifically neutralized wild 51 type OROV, and using peptide arrays we mapped multiple epitopes within an N-terminal variable 52 region of Gc recognized by the immune sera. VSV-OROV lacking this variable region of Gc was 53 also immunogenic in mice producing neutralizing sera that recognize additional regions of Gc. 54 Challenge of both sets of immunized mice with wild type OROV shows that the VSV-OROV 55 chimeras reduce wild type viral infection and suggest that antibodies that recognize the variable 56 N-terminus of Gc afford less protection than those that target more conserved regions of Gc. bioRxiv preprint doi: https://doi.org/10.1101/2021.02.19.432025; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 57 Introduction 58 Oropouche virus (OROV), first isolated in 1959 from a forest worker in Trinidad and 59 Tobago, causes a debilitating febrile illness in humans that can progress to meningitis or 60 encephalitis (1, 2). OROV is the most prevalent arbovirus after dengue in Brazil (3, 4), and is 61 currently circulating in Argentina, Bolivia, Colombia, Ecuador, and Venezuela (5-7). In urban 62 areas across the Amazon region seroprevalence rates of up to 15-33%, suggest that OROV 63 infection is underappreciated (8, 9). The virus infects a broad range of species and has both a 64 sylvatic and urban cycle. During the sylvatic cycle, the virus infects sloths, monkeys, rodents, and 65 birds, with Coquillettidia venezuelensis and Ochlerotatus serratus serving as vectors (1). In the 66 urban cycle, Culicoides paraensis and Culex quinquefasciatus serve as vectors of OROV (1), with 67 human infections paralleling increases in the vector population during the rainy season (10). 68 Infection is predominantly seen in individuals returning from forested areas (11), with limited 69 evidence of direct human to human transmission (12). Climate change, expansion and 70 dissemination of vectors, globalization of travel, and habitat loss likely contribute to increases in 71 OROV infections (13). Despite the growing dissemination of OROV, and the risks posed by this 72 emergent threat, there are currently no therapeutics to combat OROV infection. 73 Oropouche virus, a member of the family Peribunyaviridae, contains a single-stranded, 74 negative-sense RNA genome divided on three segments providing a total genome size of 11, 985 75 nucleotides. The large segment (l) encodes the large protein (L) which acts as the RNA dependent 76 RNA polymerase, the medium segment (m) encodes the viral glycoprotein complex (GPC), and 77 the small segment (s) encodes the nucleocapsid protein that sheaths the genomic and 78 antigenomic RNA. Two non-structural proteins, NSs and NSm are coded by the small and medium 79 segments, respectively. The GPC is synthesized as a single polyprotein that undergoes co- 80 translational cleavage by host-cell proteases into the two glycoproteins, Gn and Gc and liberates 81 the intervening NSm protein (14). The Gc protein acts as the viral fusogen (15), and Gn mediates 82 attachment and shields and protects Gc from premature triggering (16). Extrapolating from studies bioRxiv preprint doi: https://doi.org/10.1101/2021.02.19.432025; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 83 with La Crosse (17-20) and Schamllenberg (16, 21) viruses, both in the same orthobunyavirus 84 genus of the Peribunyaviridae, antibodies against the glycoproteins may protect against infection 85 and are therefore an important objective of vaccine strategies against OROV. 86 Vesicular stomatitis virus (VSV), the prototype of the family Rhabdoviridae, infects cells 87 by a single attachment and fusion glycoprotein (G) (22). The development of reverse genetic 88 approaches to manipulate the VSV genome (23) permitted replacement of the attachment and 89 fusion machinery with those of heterologous lipid enveloped viruses (24-28). In the case of Zaire 90 ebolavirus, the resulting VSV-ZEBOV chimera is a live attenuated vaccine, ERVEBO® that is 91 approved for use in humans (29-31). Analogous vaccine candidates are in pre-clinical and clinical 92 development for multiple enveloped viruses (25, 27, 32), including severe acute respiratory 93 syndrome 2 coronavirus (33). In addition to providing a platform for development of candidate 94 vaccines, the VSV-chimeric viruses have also permitted investigation of viral tropism, cellular 95 entry pathways, and helped understand correlates of immune protection (30, 34-38). 96 Building on this proven approach, we generate a VSV-chimera in which the native 97 glycoprotein gene is replaced by the GPC of OROV. The resulting VSV-OROV chimera replicates 98 to high-titers in BSRT7 cells in culture, and efficiently incorporates the Gn and Gc of OROV into 99 particles. Following single dose or prime-boost intramuscular injection of mice, VSV-OROV elicits 100 the production of immune specific sera that neutralize wild-type OROV. Using peptide arrays 101 corresponding to the OROV glycoproteins we find significant reactivity to the more variable N- 102 terminal domain of Gc that precedes the domains that are structurally homologous to other class 103 II fusion proteins. We generate two additional VSV-OROV chimeras lacking portions of the 104 variable N-terminus of Gc, termed the “head” and “stalk” domain. Although both variants yielded 105 replication competent virus deletion of the stalk domain led to the accumulation of mutations in 106 Gc. Immunization of mice with the VSV-OROV lacking the head domain of Gc generated immune 107 sera reactive with new regions of Gc.
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