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_++++��������������������������������������������������������������������rg+++++++++V	_:	Research article
A 39-kDa capsular protein is a major cross-protection factor demonstrated by protection of chicken with a live attenuated 
Pasteurella multocida strain P-1059 

Nattawooti Sthitmatee1, 3*, Terdsak Yano1, Kannikar Na Lampang1, 
Chaisuree Suphavilai2, Yasushi Kataoka3, Takuo Sawada3

1 Faculty of Veterinary Medicine, 2 Research Institute for Health Sciences, Chiang Mai University, Chiang Mai 50100, Thailand
3 Laboratory of Veterinary Microbiology, Nippon Veterinary and Life Science University, Musashino, Tokyo 180-8602, Japan

*CORRESPONDENCE TO: Nattawooti Sthitmatee, Department of Veterinary Bioscience and Veterinary Public Health, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai 50100, Thailand Telephone: +66-53-948-002. Fax: +66-948-041. E-mail address:  HYPERLINK "mailto:drneaw@gmail.com" drneaw@gmail.com   

  
ABSTRACT. To state that 39-kDa protein of Pasteurella multocida strain P-1059 (serovar A:3) is essential for a cross protection. Then, strain PBA322 have been constructed by inhibiting the 39-kDa protein synthesis of capsulated strain of Pasteurella multocida strain P-1059, was evaluated as a live vaccine in chickens. Strain PBA322 is a low capsulated strain in comparison with a parental strain P-1059. Chickens were vaccinated by single injection and then challenge-exposure with strains P-1059 or X-73 at two-week post vaccination. Moreover, immune responses were also evaluated for both humoral and cellular immune response by ELISA and lymphocyte proliferation assay, respectively. The results showed that the live vaccine induced efficient immunity to protect chicken from challenge-exposure with parent strain but heterologous protectivity was poor. This concluded that the 39-kDa protein is essential for a cross protection.

KEY WORDS: fowl cholera, Pasteurella multocida, 39-kDa protein, cross-protection






INTRODUCTION
	Pasteurella multocida is a gram negative bacterium and the causative agent of fowl cholera, bovine or buffalo hemorrhagic septicemia and swine atrophic rhinitis. The bacteria can be classified into 5 capsular serogroups A, B, D, E and F [20] and 16 somatic serotypes 1-16 [11]. Strains of capsular serogroup A and somatic serotypes 1, 3 and 4 are known as the causative agents of fowl cholera [20-22]. The virulence factors of P. multocida including capsular protein have been demonstrated [1,2,4,5,7,8,9,13,16,19]. Bacterial capsule plays a role to adhere to epithelial cells of host at the early stage of infection [10,13]. The 39-kDa protein in crude capsular extract (CCE) of strain P-1059 (serovar A:3) is an adhesive protein and located in the bacterial capsule [1,5]. N-terminal sequence analysis of this protein was demonstrated to be identical to the major outer membrane protein H (OmpH) of strain P-1059 [6]. The mutant strain PBA322 of P. multocida strain P-1059 has been constructed by inhibition of this 39-kDa protein synthesis [23]. Moreover, that mutant strain lost capsule synthesis is also attenuated even though the high number of bacteria was inoculated but the protectivity of chicken against challenge-exposure with the predominant strains of fowl cholera is needed to be clarified. Then, the aims of this study were to state that a 39-kDa protein or OmpH of strain P-1059 is essential for cross protection. 
 
MATERIALS AND METHODS
Bacterial strains, media and growth conditions: The bacterial strains used in this study are P. multocida strains X-73 (serovar A:1), P-1059 (serovar A:3) and PBA322 (serovar A:3) [6,23], respectively. Strain PBA322, a low capsulated strain, was constructed by inhibition of 39-kDa protein synthesis as described in the previous study [23]. P. multocida strains were grown in brain heart infusion (BHI; Becton, Dickinson and Company, Sparks, MD, USA) broth at 37(C for 6 hr and then subcultured on dextrose starch agar (DSA; Becton, Dickinson and Company) at 37(C for another 18 hr before used in the experiments.

Vaccine: Strain PBA322 from strain P-1059 was used as a live attenuated vaccine in this study. One single colony of strain PBA322 was inoculated in BHI broth and incubated at 37(C until OD600 reached 0.1. Three dosages of live vaccines were prepared by suspending bacterial cells in BHI broth and adjusted the concentration to 1 � of bacterial number at concentration of OD600. In order to enumerate the viable bacterial number, a serial tenfold dilution was performed in BHI broth before spreading onto DSA plate. Moreover, a sterile BHI broth was used as negative control vaccines. 

Chickens: Totally 40 eight-week-old layers of P. multocida-antibody-free (Hi-Sex; RPM Farm & Feed Co. Ltd., Chiang Mai, Thailand) were used in this study (Table 1). Three ml of blood was collected from all the chicken before each vaccination or challenge-exposure in order to evaluate the immune responses by enzyme-linked immunosorbent assay (ELISA) and lymphocyte proliferation assay (LPA). The use of laboratory animal was reviewed by the animal welfare committee of Faculty of Veterinary Medicine, Chiang Mai University. Experiments were performed in closed system. Experiment rooms and instruments were cleaned with disinfectant for two weeks before and after experiment. Waste products were treated before released to environment.

Vaccinations: Chicken were divided into 4 groups (group 1-4) based on the strains for challenge-exposure (Table 1). Groups 1 and 3 were vaccinated with a live vaccine as an experiment groups while groups 2 and 4 were vaccinated with a sterile BHI broth as negative groups. Chickens of groups 1 and 3 were vaccinated with a single dose of a live vaccine with the concentration of 3.3 � 108 cfu/ml. 

Determination of humoral immune response: Antibody titers were determined by the indirect ELISA [24]. Micro plates (Nunc-immunoTM plate, Denmark) were coated with 0.3% formalinized-whole cell of P. multocida strains X-73 or P-1059 in coating buffer; 0.5 M carbonate buffer (pH 9.6), and incubated at 4(C overnight. Plates were incubated with blocking buffer (1% skim milk in PBS) for 1 h to prevent the non-specific binding. Each chicken serum diluted with blocking buffer was then added into each well of the plate. After washing the plates three times with PBS-T, each well was added with a 1:1000 dilution of horseradish peroxidase-conjugated anti-chicken IgY (IgG; Sigma Aldrich, St. Louis, MO, USA) in blocking buffer. Substrate solution (30 mg O-phenylenediamine dihydrochloride: O-PDA; Wako, Japan) in substrate buffer (0.2 M Na2HPO4-12H20; 0.1 M C6H8O7; pH 4.8) was added and the reaction was stopped by adding 2 N sulfuric acid (H2SO4; Wako). Then, the absorbance values were recorded at wavelength 492 nm by ELISA reader (Immuno Mini NJ 2300, Intermed, Japan). Results were expressed as log antibody titer, calculated as (1.464 � log10 Sp value) + 3.197. The average antibody titer of each group was calculated by the standard mean and the calculated values were used to compare the statistical data.

Determination of cellular immune response: In vitro LPA was adapted and performed as described previously [14,18]. Peripheral blood mononuclear cells (PBMCs) were prepared from three ml of blood by gradient centrifugation technique [10] with Ficoll� gradient (Amersham Pharmacia Biotech, Uppsala, Sweden) and centrifuged at 400 g for 30 min. PBMCs fraction was collected and washed twice with sterile RPMI tissue culture medium (RPMI1640, 31800-022, Gibco, Invitrogen, CA) supplemented with 100 IU/ml streptomycin, and 100 IU/ml penicillin (RPMI). Subsequently, pellets were resuspended with 4 ml RPMI tissue culture medium supplemented with 100 IU/ml streptomycin, 100 IU/ml penicillin, 10 % fetal calf serum (FCS, 10270-098, Gibco) and 2.5�10-5 M 2-Mercaptoethanol (R10 culture medium) before enumerating number of cells. PBMCs at 1�106 cells/well were stimulated in triplicates with 5.0 �g/ml (final concentration) of crude capsular antigen (CCE) from strains X-73 and P-1059 in 96-well U bottom microtiter plate. R10 culture medium and 10 �g/ml of ConA (ConcanavalinA, C-2010, Sigma) were used as cell control and mitogen control, respectively. Then microtiter plate was incubated at 42�C for 48 h in a humidified atmosphere with 5% CO2. The last 16 h before harvesting, cultures were pulsed with 0.25 �Ci of methyl-[3H]-thymidine. Thymidine uptake was determined with a liquid scintillation counter (Microbeta TRILUX, Wallac, Finland). Results were expressed as stimulation indices (SI), calculated as SI = mean cpm in stimulated wells/mean cpm in media wells.

Protection assay: Chickens were challenge-exposed at two weeks post vaccination. Chicken of groups 1 and 2 were challenge-exposed with 4.3 � 104 cfu/ml of the parent strain P-1059 to determine the homologous protection while groups 3 and 4 were challenge-exposed with 2.3 � 103 cfu/ml of strain X-73 to determine the heterologous protection [24]. The birds were observed for their mortality rates and clinical signs for 10 days. 

Statistical analyses: Comparisons of protection in immunized chickens were made by the Fisher�s exact test.

RESULTS
Experiment in chickens: Groups of chickens, vaccines and results were shown in Table 1. During ten days post challenge-exposure, all chickens of groups 2 and 4 were found dead at 12 - 24 h post challenge-exposure. Necropsies were taken and samples were collected and sent to confirm cause of the death at microbiological laboratory. The carcasses showed the typical gross lesions of fowl cholera, e.g. multiple necrotic foci in liver and/or spleen, lung congestion and edema, multiple petechiae in liver, hemorrhage in the small intestines and splenomegaly. Chickens in the experimental groups began to show the clinical sign, for examples; depression, inappetite, at 6 to 8 h after challenge-exposure. Then, at 12 h after challenge-exposure, chickens started to die, and dead chickens were found until three days after challenge-exposure. Bacterial isolation showed pure colonies on the agar plates and biochemical reactions of the isolates showed the typical properties of P. multocida (data not shown). 

Protection assay: Chickens in group 1 was challenge-exposed with the parent strain of the vaccine; strain P-1059 and complete protection (100% survivor) was obtained. In contrast, no survivor (0%) was observed in group 3 that were challenge-exposed with strain X-73. Fisher�s exact test indicated that there was significant difference in cross-protection conferred by a live vaccine (P<0.05). 

ELISA: The average log antibody titers of chicken antiserum against strains P-1059 and X-73 were shown in Figs. 1-2. Chicken�s antibody titers of all groups at pre-vaccination were not significantly different (P=0.13). Antibody titers were elevated in vaccinated chickens at 2-weeks post immunization. In contrast, antibody titers of the non-vaccinated control group were not elevated. Moreover, antibody response of vaccinated chickens was significantly different to non-vaccinated group (P<0.05). 

LPA: The LPA data are shown in Figs. 3-4. The responses of all group pre-vaccination when stimulated with 5 �g/ml of P. multocida strains P-1059 or X-73 antigens were not significantly different (P=0.21). The LPA post-vaccination when stimulated with 5 �g/ml of P. multocida strain P-1059 antigen showed significant difference to the LPA of the stimulation with P. multocida strain X-73 antigen (P<0.05).  

DISCUSSION
	Since, the mutant PBA322 lacks of the 39-kDa protein, this might affect to the cross protection. The previously investigation indicated that the 39-kDa and recombinant 39-kDa proteins are cross-protective adhesive antigens of P. multocida capsular serogroup A strains [4,24]. Then, existing of the 39-kDa protein in capsule of bacteria corresponds to be bacterial cross-protective immunogen. As expected, the low protection conferred by the heterologous challenge-exposure. The previous study constructed and determined the protection conferred by mutants of P. multocida [12,15]. Those entire previous studies constructed mutant based on other gene excluded the cross-protective protein like our mutant. The acapsular P. multocida strain PBA930, a hexA::tet(M) mutant, was able to protect chicken against challenge with wild type strain X-73 [12]. Moreover, the attenuated aroA mutant PMP3 gave efficient protectivity against challenge with strains X-73 and P-1662 [15]. Therefore, the present protection assays conclude that the inhibition of 39-kDa protein synthesis causes a thin encapsulated strain but that strain may lack of a cross- protective characteristic.       
	The live noncapsulated mutants were attenuated and also proved to be efficacious live-vaccine candidates for mice and the natural hosts [12,15]. Theoretically, live vaccine activates all phases of immune system. They elicit humoral IgG and local IgA, raise immune response to all protective antigens, offer more durable immunity and are more cross-reactive. Thus they stimulate antibodies against multiple epitopes which are similar to those elicited by the wild type. As the results, antibody titer profiles showed low antibody response in strain X-73-coated ELISA, but in contrast, very high response in strains P-1059 or PBA322-coated ELISA. This correlated to the characteristic of the strain. In our previous knowledge, strain PBA322 was constructed by inhibition of this cross-protective antigen; a cross-protective antigen among P. multocida capsular type A strains [23], and subsequently, a cross-protective character of the strain must be deleted. Therefore, the antibody induced by vaccination with strain PBA322 reacted particularly to homologous strain. LPA results indicated that the lymphocyte of chicken vaccinated with the mutant was not correlated to the protectivity. LPA profiles showed low proliferation of lymphocyte after vaccination. Indeed, live vaccine induces greater lymphocyte response than a killed vaccine. Role of the cellular immune response in the protection still be questioned even though the bacterium has been demonstrated as an intracellular bacterium [3,16]. The previous study suggested that there is no evidence of a major role of cell-mediated immunity induced by P. multocida vaccine for hemorrhagic septicemia because P. multocida has not been described as an intracellular pathogen [25]. In contrast, Ibrahim et al. [16] and Al-haj Ali et al. [3] characterized the ability of P. multocida to penetrate to host cells and their results suggested that P. multocida might be an intracellular pathogen. Ibrahim et al. [16] reported that P. multocida could multiply intracellular in hepatocyte or heart tissue of host and employing the glycoprotein as an invasive factor to receptor at chicken embryo fibroblast cells surface [3]. However, the intracellular multiplication and cellular immune response of the bacterium needed to be clarified. 
In conclusion, a cross-protection conferred by vaccination with a live vaccine, a 39-kDa protein knock-out strain, was poor and the results stated that a 39-kDa protein of P. multocida is essential for a cross-protection. Moreover, the cross-protection is mainly owing to humoral immunity even the bacterium is able to multiply intracellular.

ACKNOWLEDGEMENTS. The authors would like to express our appreciations deeply to staffs at the Research Institute for Health Sciences (RIHES), Chiang Mai University for their laboratory assistance and also to Dr. Suvit Chotinun of the Avian Clinic, Faculty of Veterinary Medicine, Chiang Mai University for his kind assistance. This research was granted by Research Administration Center, Chiang Mai University fiscal year 2008-2009.

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