Abstract
This study was conducted to determine the immunostimulatory effect of l-proline on inactivated vaccine immunized mice. Ninety-five female KM mice were randomly divided into five groups: (1) mice received dietary supplementation with 0.4 % l-proline and immunized with inactivated vaccine (V–P group); (2) mice received dietary supplementation with 0.3 % l-alanine (isonitrogenous control) and immunized with inactivated vaccine (V–A group, negative control); (3) mice were immunized with inactivated vaccine with oil adjuvant (V–O group, positive control); (4) mice were immunized with inactivated vaccine with aluminum hydroxide adjuvant (V–H group, positive control); (5) mice immunized with phosphate-buffered saline (control group). All mice were dead in the control group between 36 and 48 h post infection. Mice in the V–P group showed 100 % protection after challenge with P. multocida serotype A (CQ2) at dose of 4.4 × 105 CFU (2LD50). Meanwhile, serum antibody titers in the V–P group were higher than those in the V–A group before infection and those in the V–A and V–O groups at 36 h post infection. Moreover, serum IL-1β levels in the V–P group were lower than those in V–O group. Furthermore, serum GSH-PX levels in the V–P group were higher than those in the V–A and V–O groups. Collectively, dietary proline supplementation confers beneficial immunostimulatory effects in inactivated P. multocida vaccine immunized mice.
Similar content being viewed by others
Abbreviations
- BSA:
-
Bovine serum albumin
- GSH-PX:
-
Glutathione peroxidase
- IL:
-
Interleukin
- PBS:
-
Phosphate-buffered saline
- TNF-α:
-
Tumor necrosis factor alpha
References
Baggiolini M, Loetscher P, Moser B (1995) Interleukin-8 and the chemokine family. Int J Immunopharmacol 17:103–108
Biffl WL, Moore EE, Moore FA et al (1996) Interleukin-6 in the injured patient. Marker of injury or mediator of inflammation? Ann Surg 224:647–664
Bronte V, Serafini P, Mazzoni A et al (2003) l-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol 24:302–306
Clapp T, Siebert P, Chen D et al (2011) Vaccines with aluminum-containing adjuvants: optimizing vaccine efficacy and thermal stability. J Pharm Sci 100:388–401
Dai ZL, Li XL, Xi PB et al (2012a) Regulatory role for l-arginine in the utilization of amino acids by pig small-intestinal bacteria. Amino Acids 43:233–244
Dai ZL, Li XL, Xi PB et al (2012b) Metabolism of select amino acids in bacteria from the pig small intestine. Amino Acids 42:1597–1608
Dinarello CA (1997) Interleukin-1. Cytokine Growth Factor Rev 8:253–265
Duval D, Demangel C, Munier-Jolain K et al (1991) Factors controlling cell proliferation and antibody production in mouse hybridoma cells: I. Influence of the amino acid supply. Biotechnol Bioeng 38:561–570
Gao KG, Jiang ZY, Lin YC et al (2012) Dietary l-arginine supplementation enhances placental growth and reproductive performance in sows. Amino Acids 42:2207–2214
Goto N, Kato H, Maeyama J et al (1993) Studies on the toxicities of aluminium hydroxide and calcium phosphate as immunological adjuvants for vaccines. Vaccine 11:914–918
Hou YQ, Wang L, Ding BY et al (2011) Alpha-ketoglutarate and intestinal function. Front Biosci 16:1186–1196
Hou Y, Wang QL, Zhang W et al (2012) Protective effects of N-acetylcysteine on intestinal functions of piglets challenged with lipopolysaccharide. Amino Acids 43:1233–1242
Kaul S, Sharma SS, Mehta IK (2008) Free radical scavenging potential of l-proline: evidence from in vitro assays. Amino Acids 34:315–320
Li P, Yin YL, Li D et al (2007) Amino acids and immune function. Br J Nutr 98:237–252
Li P, Mai KS, Trushenski J et al (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53
Li XL, Rezaei R, Li P et al (2011) Composition of amino acids in feed ingredients for animal diets. Amino Acids 40:1159–1168
Liu XD, Wu X, Yin YL et al (2012) Effects of dietary l-arginineor N-carbamylglutamate supplementation during late gestation of sows on the miR-15b/16, miR-221/222, VEGFA and eNOS expression in umbilical vein. Amino Acids 42:2111–2119
Munder M, Schneider H, Luckner C et al (2006) Suppression of T-cell functions by human granulocyte arginase. Blood 108:1627–1634
Naugler WE, Karin M (2008) The wolf in sheep’s clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trends Mol Med 14:109–119
Peranzoni E, Marigo I, Dolcetti L et al (2007) Role of arginine metabolism in immunity and immunopathology. Immunobiology 212:795–812
Phang JM, Liu W (2012) Proline metabolism and cancer. Front Biosci 17:1835–1845
Phang JM, Donald SP, Pandhare J et al (2008) The metabolism of proline, a stress substrate, modulates carcinogenic pathways. Amino Acids 35:681–690
Phang JM, Liu W, Zabirnyk O (2010) Proline metabolism and microenvironmental stress. Annu Rev Nutr 30:441–463
Praveena PE, Periasamy S, Kumar AA et al (2010) Cytokine profiles, apoptosis and pathology of experimental Pasteurella multocida serotype A1 infection in mice. Res Vet Sci 89:332–339
Ren W, Luo W, Wu M et al (2011) Dietary l-glutamine supplementation improves pregnancy outcome in mice infected with type-2 porcine circovirus. Amino Acids. doi:10.1007/s00726-011-1134-5
Ren W, Yin Y, Liu G et al (2012a) Effect of dietary arginine supplementation on reproductive performance of mice with porcine circovirus type 2 infection. Amino Acids 42:2089–2094
Ren W, Zou L, Li N et al (2012b) Dietary arginine supplementation enhances immune responses to inactivated Pasteurella multocida vaccination in mice. Br J Nutr 109:867–872
Ren W, Yu R, Liu G et al (2013a) DNA vaccine encoding the major virulence factors of Shiga toxin type 2e (Stx2e)-expressing Escherichia coli induces protection in mice. Vaccine 31:367–372
Ren W, Wu M, Wei L et al (2013b) Dietary supplementation with proline confers a positive effect in both porcine circovirus-infected pregnant and non-pregnant mice. Br J Nutr. doi:10.1017/S0007114513000652
Rezaei R, Knabe DA, Li XL et al (2011) Enhanced efficiency of milk utilization for growth in surviving low-birth-weight piglets. J Anim Sci Biotech 2:73–83
Rezaei R, Wang WW, Wu ZL et al (2013a) Biochemical and physiological bases for utilization of dietary amino acids by young pigs. J Anim Sci Biotech 4:7
Rezaei R, Knabe DA, Tekwe CD et al (2013b) Dietary supplementation with monosodium glutamate is safe and improves growth performance in postweaning pigs. Amino Acids 44:911–923
Rodriguez PC, Zea AH, DeSalvo J et al (2003) l-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J Immunol 171:1232–1239
Shi W, Meininger CJ, Haynes TE et al (2004) Regulation of tetrahydrobiopterin synthesis and bioavailability in endothelial cells. Cell Biochem Biophys 41:415–434
Sun Y, Li M, Liu J (2008) Haemolytic activities and adjuvant effect of Anemone raddeana saponins (ARS) on the immune responses to ovalbumin in mice. Int Immunopharmacol 8:1095–1102
Tan BE, Yin YL, Liu ZQ et al (2009) Dietary l-arginine supplementation increases muscle gain and reduces body fat mass in growing-finishing pigs. Amino Acids 37:169–175
Tan BE, Yin YL, Liu ZQ et al (2011) Dietary l-arginine supplementation differentially regulates expression of fat-metabolic genes in porcine adipose tissue and skeletal muscle. J Nutr Biochem 22:441–445
Tan BE, Li XG, Yin YL et al (2012a) Regulatory roles for l-arginine in reducing white adipose tissue. Front Biosci 17:2237–2246
Tan BE, Li XG, Wu G et al (2012b) Dynamic changes in blood flow and oxygen consumption in the portal-drained viscera of growing pigs receiving acute administration of l-arginine. Amino Acids 43:2481–2489
Townsend KM, Boyce JD, Chung JY et al (2001) Genetic organization of Pasteurella multocida cap Loci and development of a multiplex capsular PCR typing system. J Clin Microbiol 39:924–929
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759
Wang XQ, Ou DY, Yin JD et al (2009) Proteomic analysis reveals altered expression of proteins related to glutathione metabolism and apoptosis in the small intestine of zinc oxide-supplemented piglets. Amino Acids 37:209–218
Wang JJ, Wu ZL, Li DF et al (2012) Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal 17:282–301
Wei JW, Carroll RJ, Harden KK et al (2012) Comparisons of treatment means when factors do not interact in two-factorial studies. Amino Acids 42:2031–2035
Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17
Wu G (2010a) Recent advances in swine amino acid nutrition. J Anim Sci Biotech 1:49–61
Wu G (2010b) Functional amino acids in growth, reproduction and health. Adv Nutr 1:31–37
Wu G, Fang YZ, Yang S et al (2004) Glutathione metabolism and its implications for health. J Nutr 134:489–492
Wu G, Bazer FW, Datta S et al (2008) Proline metabolism in the conceptus: implications for fetal growth and development. Amino Acids 35:691–702
Wu G, Bazer FW, Burghardt RC et al (2011) Proline and hydroxyproline metabolism: implications for animal and human nutrition. Amino Acids 40:1053–1063
Wu G, Wu ZL, Dai ZL et al (2013) Dietary requirements of “nutritionally nonessential amino acids” by animals and humans. Amino Acids 44:1107–1113
Xi PB, Jiang ZY, Dai ZL et al (2012) Regulation of protein turnover by l-glutamine in porcine intestinal epithelial cells. J Nutr Biochem 23:1012–1017
Yao K, Yin YL, Chu WY et al (2008) Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. J Nutr 138:867–872
Yao K, Yin YL, Li XL et al (2012) Alpha-ketoglutarate inhibits glutamine degradation and enhances protein synthesis in intestinal porcine epithelial cells. Amino Acids 42:2491–2500
Yin YL, Tang ZR, Sun ZH et al (2008) Effect of galacto-mannan-oligosaccharides or chitosan supplementation on cytoimmunity and humoral immunity response in early-weaned piglets. Asian Aust J Anim Sci 21:723–731
Yin FG, Zhang ZZ, Huang J et al (2010) Digestion rate of dietary starch affects systemic circulation of amino acids in weaned pigs. Br J Nutr 103:1404–1412
Zablocka A, Ogorzalek A, Macala J et al (2010) A proline-rich polypeptide complex (PRP) influences inducible nitric oxide synthase in mice at the protein level. Nitric Oxide 23:20–25
Acknowledgments
This research was jointly supported by MATS-Beef Cattle Yak system(CARS-38), National Basic Research Program of China (2012CB124704, 2013CB127301), National Natural Science Foundation of China (31110103909,30901040, 31272463, 30928018, and 31101729), the State Key Laboratory of Food Science and Technology, the Nanchang University project (SKLF-TS-201108, SKLF-KF-201005, SKLF-KF-201216), the CAS/SAFEA International Partnership Program for Creative Research Teams, Chinese Universities Scientific Funds (2012RC024), and the Thousand-People-Talent program at China Agricultural University, Texas AgriLife Research project (H-8200).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding authors
Additional information
W. Ren and L. Zou contributed equally to this study.
Rights and permissions
About this article
Cite this article
Ren, W., Zou, L., Ruan, Z. et al. Dietary l-proline supplementation confers immunostimulatory effects on inactivated Pasteurella multocida vaccine immunized mice. Amino Acids 45, 555–561 (2013). https://doi.org/10.1007/s00726-013-1490-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-013-1490-4