Differential Expression of Interleukin-8 by Polymorphonuclear Leukocytes of Two Closely Related Species, Ovis canadensis and Ovis aries, in Response to Mannheimia haemolytica Infection

ABSTRACTThe pneumonic lesions and mortality caused byMannheimia haemolyticain bighorn sheep (BHS;Ovis canadensis) are more severe than those in the related species, domestic sheep (DS;Ovis aries), under both natural and experimental conditions. Leukotoxin (Lkt) and lipopolysaccharide (LPS) are the most important virulence factors of this organism. One hallmark of pathogenesis of pneumonia is the influx of polymorphonuclear leukocytes (PMNs) into the lungs. Lkt-induced cytolysis of PMNs results in the release of cytotoxic compounds capable of damaging lung tissue. Interleukin-8 (IL-8) is a potent PMN chemoattractant. The objective of the present study was to determine if there is differential expression of IL-8 by the macrophages and PMNs of BHS and DS in response toM. haemolytica. Macrophages and PMNs of BHS and DS were stimulated with heat-killedM. haemolyticaor LPS. IL-8 expression by the cells was measured by enzyme-linked immunosorbent assays and real-time reverse transcription-PCR (RT-PCR). The PMNs of BHS expressed severalfold higher levels of IL-8 than those of DS upon stimulation. Lesional lung tissue ofM. haemolytica-infected BHS contained significantly higher levels of IL-8 than nonlesional tissue. The bronchoalveolar lavage (BAL) fluid of infected BHS also contained higher levels of IL-8 than that of infected DS. Depletion of IL-8 reduced migration of PMNs toward BAL fluid by approximately 50%, indicating that IL-8 is integral to PMN recruitment to the lung duringM. haemolyticainfection. Excessive production of IL-8, enhanced recruitment of PMNs, and PMN lysis by Lkt are likely responsible for the severity of the lung lesions inM. haemolytica-infected BHS.

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Comparison of Passively Transferred Antibodies in Bighorn and Domestic Lambs Reveals One Factor in Differential Susceptibility of These Species to Mannheimia haemolytica-Induced Pneumonia

Clinical and Vaccine Immunology ◽

10.1128/cvi.00044-11 ◽

2011 ◽

Vol 18 (7) ◽

pp. 1133-1138 ◽

Cited By ~ 11

Author(s):

Caroline N. Herndon ◽

Sudarvili Shanthalingam ◽

Donald P. Knowles ◽

Douglas R. Call ◽

Subramaniam Srikumaran

Keyword(s):

Differential Susceptibility ◽

Critical Factor ◽

Surface Antigens ◽

Ovis Canadensis ◽

Ovis Aries ◽

Mannheimia Haemolytica ◽

Domestic Sheep ◽

Experimental Conditions ◽

Content Type ◽

Impaired Ability

ABSTRACTMannheimia haemolyticaconsistently causes fatal bronchopneumonia in bighorn sheep (BHS;Ovis canadensis) under natural and experimental conditions. Leukotoxin is the primary virulence factor of this organism. BHS are more susceptible to developing fatal pneumonia than the related speciesOvis aries(domestic sheep [DS]). In BHS herds affected by pneumonia, lamb recruitment is severely impaired for years subsequent to an outbreak. We hypothesized that a lack of maternally derived antibodies (Abs) againstM. haemolyticaprovides an immunologic basis for enhanced susceptibility of BH lambs to population-limiting pneumonia. Therefore, the objective of this study was to determine the titers of Abs directed againstM. haemolyticain the sera of BH and domestic lambs at birth through 12 weeks of age. Results revealed that BH lambs had approximately 18-fold lower titers of Ab against surface antigens ofM. haemolyticaand approximately 20-fold lower titers of leukotoxin-neutralizing Abs than domestic lambs. The titers of leukotoxin-neutralizing Abs in the serum and colostrum samples of BH ewes were approximately 157- and 50-fold lower than those for domestic ewes, respectively. Comparatively, the higher titers of parainfluenza 3 virus-neutralizing Abs in the BH lambs ruled out the possibility that these BHS had an impaired ability to passively transfer Abs to their lambs. These results suggest that lower levels of leukotoxin-neutralizing Abs in the sera of BH ewes, and resultant low Ab titers in their lambs, may be a critical factor in the poor lamb recruitment in herds affected by pneumonia.

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Differential Susceptibility of Bighorn Sheep (Ovis canadensis) and Domestic Sheep (Ovis aries) Neutrophils to Mannheimia haemolytica Leukotoxin is not due to Differential Expression of Cell Surface CD18

Journal of Wildlife Diseases ◽

10.7589/2016-11-244 ◽

2017 ◽

Vol 53 (3) ◽

pp. 625-629 ◽

Cited By ~ 1

Author(s):

Rohana P. Dassanayake ◽

Sudarvili Shanthalingam ◽

Weiguo Liu ◽

Eduardo Casas ◽

Subramaniam Srikumaran

Keyword(s):

Cell Surface ◽

Differential Expression ◽

Differential Susceptibility ◽

Bighorn Sheep ◽

Ovis Canadensis ◽

Ovis Aries ◽

Mannheimia Haemolytica ◽

Domestic Sheep

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TRANSMISSION OF MANNHEIMIA HAEMOLYTICA FROM DOMESTIC SHEEP (OVIS ARIES) TO BIGHORN SHEEP (OVIS CANADENSIS): UNEQUIVOCAL DEMONSTRATION WITH GREEN FLUORESCENT PROTEIN-TAGGED ORGANISMS

Journal of Wildlife Diseases ◽

10.7589/0090-3558-46.3.706 ◽

2010 ◽

Vol 46 (3) ◽

pp. 706-717 ◽

Cited By ~ 23

Author(s):

Paulraj K. Lawrence ◽

Sudarvili Shanthalingam ◽

Rohana P. Dassanayake ◽

Renuka Subramaniam ◽

Caroline N. Herndon ◽

...

Keyword(s):

Green Fluorescent Protein ◽

Fluorescent Protein ◽

Bighorn Sheep ◽

Ovis Canadensis ◽

Ovis Aries ◽

Mannheimia Haemolytica ◽

Domestic Sheep ◽

Green Fluorescent

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Mannheimia haemolytica serotype A1 exhibits differential pathogenicity in two related species, Ovis canadensis and Ovis aries

Veterinary Microbiology ◽

10.1016/j.vetmic.2008.07.015 ◽

2009 ◽

Vol 133 (4) ◽

pp. 366-371 ◽

Cited By ~ 47

Author(s):

Rohana P. Dassanayake ◽

Sudarvili Shanthalingam ◽

Caroline N. Herndon ◽

Paulraj K. Lawrence ◽

E. Frances Cassirer ◽

...

Keyword(s):

Related Species ◽

Ovis Canadensis ◽

Ovis Aries ◽

Mannheimia Haemolytica

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Differential pulmonary immunopathologic response of domestic sheep (Ovis aries) and bighorn sheep (Ovis canadensis) to Mycoplasma ovipneumoniae infection: a retrospective study

10.1101/703249 ◽

2019 ◽

Author(s):

Paige C. Grossman ◽

David A. Schneider ◽

Donald P. Knowles ◽

Margaret A. Highland

Keyword(s):

Retrospective Study ◽

Lung Tissue ◽

Bighorn Sheep ◽

Ovis Canadensis ◽

Ovis Aries ◽

Respiratory Pathogen ◽

Domestic Sheep ◽

Lung Sample ◽

Ffpe Tissues ◽

Mycoplasma Ovipneumoniae

AbstractMycoplasma ovipneumoniae is a respiratory pathogen that can impact domestic sheep (Ovis aries; DS) and bighorn sheep (Ovis canadensis; BHS). Experimental and field data have indicated BHS are more susceptible than DS to developing polymicrobial pneumonia associated with Mycoplasma ovipneumoniae infection. We hypothesized that DS and BHS have a differential immunopathologic pulmonary response to M. ovipneumoniae infection. A retrospective study was performed using formalin-fixed, paraffin-embedded (FFPE) lung tissue from DS and BHS without and with M. ovipneumoniae detected in the lung tissue (n=8 per group). While each M. ovipneumoniae positive lung sample had microscopic changes typical of infection, including hyperplasia of intrapulmonary bronchus-associated lymphoid tissue (BALT) and respiratory epithelium, DS exhibited a more robust and well-organized BALT formation as compared to BHS. Immunohistochemistry was performed with antibodies reactive in FFPE tissues and specific for leukocyte and cytokine markers: T cell marker CD3, B cell markers CD20 and CD79a, macrophage markers CD163 and Iba1, and cytokine IL-17. Digital analysis was used to quantitate chromogen deposition in regions of interest (ROIs), including alveolar and bronchiolar areas, and bronchiolar subregions (epithelium and BALT). Main effects and interaction of species and infection status were analyzed by beta regression and Bonferroni corrections were performed on pairwise comparisons (PBon<0.05 significance). Significant species differences were identified for bronchiolar CD3 (PBon=0.0023) and CD163 (PBon=0.0224), alveolar CD163 (PBon=0.0057), and for IL-17 in each of the ROIs (alveolar: PBon=0.0009; BALT: PBon=0.0083; epithelium: PBon=0.0007). Infected BHS had a higher abundance of bronchiolar CD3 (PBon=0.0005) and CD163 (PBon=0.0162), and alveolar CD163 (PBon=0.0073). While IL-17 significantly increased with infection in BHS BALT (PBon=0.0179) and alveolar (0.0006) ROIs, abundance in DS showed an insignificant decrease in these ROIs and a significant decrease in epithelial abundance (PBon=0.0019). These findings support the hypothesis that DS and BHS have a differential immunopathologic response to M. ovipneumoniae infection.

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Differences in leukocyte differentiation molecule abundances on domestic sheep (Ovis aries) and bighorn sheep (Ovis canadensis) neutrophils identified by flow cytometry

Comparative Immunology Microbiology and Infectious Diseases ◽

10.1016/j.cimid.2016.04.006 ◽

2016 ◽

Vol 46 ◽

pp. 40-46 ◽

Cited By ~ 7

Author(s):

Margaret A. Highland ◽

David A. Schneider ◽

Stephen N. White ◽

Sally A. Madsen-Bouterse ◽

Donald P. Knowles ◽

...

Keyword(s):

Flow Cytometry ◽

Bighorn Sheep ◽

Ovis Canadensis ◽

Ovis Aries ◽

Domestic Sheep

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Progesterone promotes fetal growth in a restricted interspecies gestation (Ovis canadensis x Ovis aries)

Veterinaria México OA ◽

10.22201/fmvz.24486760e.2018.3.507 ◽

2018 ◽

Vol 5 (3) ◽

Author(s):

Octavio Mejía Villanueva ◽

Verónica Hernández Cazadero ◽

Clara Murcia Mejía ◽

Susana Rojas Maya ◽

Cristina Castaño García ◽

...

Keyword(s):

Ex Situ Conservation ◽

Treated Group ◽

Ovis Canadensis ◽

Ovis Aries ◽

Ex Situ ◽

Domestic Sheep ◽

Foetal Growth ◽

Daily Dose ◽

Hybrid Embryo ◽

Lower Fertility

Progesterone promotes foetal growth in a restricted interspecies gestation (Ovis canadensis × Ovis aries). Veterinaria México OA. 2018;5(3).Gestations between bighorn (Ovis canadensis) and domestic sheep (O. aries) can be considered for ex situ conservation of bighorn. In the first experiment, domestic sheep were inseminated with bighorn or domestic semen. Bighorn inseminated sheep showed lower fertility than domestic inseminated sheep (40% vs. 65%, p = 0.11). Bighorn inseminated sheep had longer gestation periods (152.13 days vs. 146.54 days, p < 0.001) and lower progesterone levels during the last third. Hybrid lambs weighed less than domestic lambs (2.46 kg vs. 5.10 kg, p < 0.001). Their placentas were not as long (48.67 cm vs. 72.17 cm, p < 0.001), were less wide (17.83 cm vs. 23.83 cm, p < 0.001), and the weight of cotyledons was lower (1.50 g vs. 3.20 g, p < 0.001). In the second experiment, hybrid embryos (O. canadensis × O. aries) were transferred into domestic recipients, and pregnant ewes were divided into the treated group, which had a progesterone daily dose of 25 mg from weeks 7 to 20, and the non treated group. Gestation in domestic sheep that received one hybrid embryo and progesterone reached 152.60 days, which was similar to the 153.33 days (p = 0.51) in the non treated sheep. Hybrid offspring of the group treated with progesterone were heavier, 3.41 kg, than the control, 2.21 kg (p < 0.001), and their placentas were longer (71.20 vs. 50.83 cm, p = 0.002). Although progesterone levels were lower in domestic females inseminated with bighorn and in the recipients of hybrid embryos, it is possible to establish pregnancies between both species and the birth of viable offspring. The administration of progesterone during gestation increases the length of the placenta and promotes higher birth weights of hybrids.Figure 1. Progesterone (ng/mL) in interspecies gestations (O. c. mexicana × O. aries, n = 6) and intraspecies gestations (O. aries × O. aries, n = 6).*Statistically different values (p < 0.01).

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Identification of novel variants of interferon-tau gene in Bighorn sheep (Ovis canadensis mexicana), Pelibuey sheep (Ovis aries) and its expression in hybrid blastocysts (Ovis canadensis × Ovis aries)

Canadian Journal of Animal Science ◽

10.4141/cjas2011-023 ◽

2012 ◽

Vol 92 (3) ◽

pp. 275-283 ◽

Cited By ~ 1

Author(s):

M. Palma-Irizarry ◽

P. Damian-Matsumura ◽

M. Betancourt ◽

S. Romo ◽

G. Perales ◽

...

Keyword(s):

Bighorn Sheep ◽

Ovis Canadensis ◽

Ovis Aries ◽

Domestic Sheep ◽

Interferon Tau ◽

Pelibuey Sheep ◽

Novel Variants ◽

Ovis Canadensis Mexicana

Palma-Irizarry, M., Damian-Matsumura, P., Betancourt, M., Romo, S., Perales, G., Lagunas-Martínez, A., Madrid-Marina, M. V., Mejía, O. and Ducolomb, Y. 2012. Identification of novel variants of interferon-tau gene in Bighorn sheep ( Ovis canadensis mexicana ), Pelibuey sheep ( Ovis aries ) and its expression in hybrid blastocysts ( Ovis canadensis×Ovis aries ). Can. J. Anim. Sci. 92: 275–283. The major signal for maternal recognition of pregnancy (MRP) in ruminants is interferon-tau (IFNT). Four novel sequences of the IFNT gene were isolated from genomic DNA obtained from blood samples of Bighorn, Pelibuey or the hybrid ewes. The deduced amino acid sequence of the hybrid ewe showed 100% identity with one Bighorn sheep IFNT sequence, suggesting that this sequence was inherited from Bighorn sheep. The high degree of identity between Pelibuey and Bighorn sheep sequences could be a possible explanation for the successful MRP in some Bighorn hybrid pregnancies. In vivo and in vitro domestic sheep (Ovis aries) and hybrid sheep (Ovis aries×Ovis canadensis) blastocysts were obtained, and IFNT expression was measured by semiquantitative RT-PCR. In vivo and in vitro hybrid blastocysts showed lower expression of IFNT when compared with domestic blastocysts. In conclusion this study showed that there exists an effect of hybridization on IFNT expression and this can affect the MRP.

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