Dietary l-arginine supplementation enhances the immune status in early-weaned piglets (original) (raw)

Abstract

This study was conducted to test the hypothesis that dietary L-arginine supplementation enhances immunity in early weaned piglets. Seventy piglets weaned at 7 days of age were assigned to five groups (14 pigs/group), representing supplementation of 0.0, 0.2, 0.4, 0.6, and 0.8% l-arginine to a milk-based formula. On Day 7 after initiation of treatment, spleen weight in piglets supplemented with 0.2 and 0.8% arginine was heavier and thymus size was larger in piglets supplemented with 0.6% arginine, whereas serum concentration of immunoglobulin (Ig) M was higher but that of IL-8 was lower in piglets supplemented with 0.6 and 0.8% arginine, compared with the control group. Dietary supplementation with 0.8% arginine increased the numbers of white blood cells and granulocytes, and gene expression of interleukin (IL)-8 in spleen. On Day 14, compared with control piglets, granulocyte numbers were greater but lymphocyte numbers were lower in piglets supplemented with 0.2 and 0.4% arginine, whereas splenic expression of IL-8 and tumor necrosis factor-α genes was increased in piglets supplemented with 0.8% arginine. Additionally, IgG and IgM concentrations in serum and growth performance were greater in piglets supplemented with 0.4–0.8% arginine, compared with unsupplemented piglets. Collectively, dietary supplementation with 0.4–0.8% l-arginine for 2 weeks enhances both cellular and humoral immunity in piglets by modulating the production of leukocytes, cytokines and antibodies. These results indicate that increasing l-arginine provision is beneficial for optimal immune responses in young pigs and also have important implications for designing the next generation of improved formula for human infants.

Access this article

Log in via an institution

Subscribe and save

• Get 10 units per month
• Download Article/Chapter or eBook
• 1 Unit = 1 Article or 1 Chapter
• Cancel anytime Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Ig:

Immunoglobulin

IL:

Interleukin

NO:

Nitric oxide

RT-PCR:

Real-time polymerase-chain reaction

TNF:

Tumor necrosis factor

References

• Barbul A, Wasserkrug HL, Sisto DA, Seifter E, Rettura G, Levenson SM, Efron G (1980) Thymic stimulatory actions of arginine. J Parenter Enteral Nutr 4:446–449
  Article CAS Google Scholar
• Broxmeyer HE, Cooper S, Cacalano G, Hague NL, Baillish E, Moore MW (1996) Involvement of interleukin (IL) 8 receptor in negative regulation of myeloid progenitor cells in vivo: evidence from mice lacking the murine IL-8 receptor homologue. J Exp Med 184:1825–1832
  Article PubMed CAS Google Scholar
• Daly JM, Reynolds J, Thom A, Kinsley L, Dietrick-Gallagher M, Shou J, Ruggieri B (1988) Immune and metabolic effects of arginine in the surgical patient. Ann Surg 208:512–523
  Article PubMed CAS Google Scholar
• Deng ZY, Zhang JW, Wu GY, Yin YL, Ruan Z, Li TJ, Chu WY, Kong XF, Zhang YM, Fan YW, Liu R, Huang RL (2007) Dietary supplementation with polysaccharides from Semen cassiae enhances immunoglobulin production and interleukin gene expression in early-weaned piglets. J Sci Food Agric 87:1868–1873
  Article CAS Google Scholar
• Dong GZ, Pluske JR (2007) The low feed intake in early-weaned pigs: problems and possible solutions. Asian Aust J Anim Sci 20:440–452
  CAS Google Scholar
• Escobar J, Van Alstine WG, Baker DH, Johnson RW (2004) Decreased protein accretion in pigs with viral and bacterial pneumonia is associated with increased myostatin expression in muscle. J Nutr 134:3047–3053
  PubMed CAS Google Scholar
• Evoy D, Fahey TJ, Daly JM (1998) Immunonutrition: the role of arginine. Nutrition 14:611–617
  Article PubMed CAS Google Scholar
• Flynn NE, Meininger CJ, Kelly K, Ing NH, Morris SM Jr, Wu G (1999) Glucocorticoids mediate the enhanced expression of intestinal type II arginase and argininosuccinate synthase in postweaning pigs. J Nutr 129:799–803
  PubMed CAS Google Scholar
• Flynn NE, Meininger CJ, Haynes TE, Wu G (2002) The metabolic basis of arginine nutrition and pharmacotherapy. Biomed Pharmacother 56:427–438
  Article PubMed CAS Google Scholar
• Frank JW, Escobar J, Hguyen HV, Jobgen SC, Jobgen WS, Davis TA, Wu G (2007) Oral _N_-carbamylglutamate supplementation increases protein synthesis in skeletal muscle of piglets. J Nutr 137:315–319
  PubMed CAS Google Scholar
• Fu WJ, Hu J, Spencer T, Carroll R, Wu G (2006) Statistical models in assessing fold changes of gene expression in real-time RT-PCR experiments. Comput Biol Chem 30:21–26
  Article PubMed CAS Google Scholar
• Holtenius K, Persson-Waller K, Essen-Gustavsson B, Holtenius P, Hallen SC (2004) Metabolic parameters and blood leukocyte profiles in cows from herds with high or low mastitis incidence. Vet J 168:65–73
  PubMed CAS Google Scholar
• Hu CA, Khalil S, Zhaorigetu S, Liu Z, Tyler M, Wan G, Valle D (2008) Human ∆1-pyrroline-5-carboxylate synthase: function and regulation. Amino Acids. doi:10.1007/s00726-008-0075-0
• Jobgen WS, Fried SK, Fu WJ, Meininger CJ, Wu G (2006) Regulatory role for the arginine-nitric oxide pathway in metabolism of energy substrates. J Nutr Biochem 17:571–588
  Article PubMed CAS Google Scholar
• Johnsona IR, Ball RO, Baracos VE, Field CJ (2006) Glutamine supplementation influences immune development in the newly weaned piglet. Dev Comp Immunol 30:1191–1202
  Article Google Scholar
• Kelly E, Morris SM Jr, Billiar TR (1995) Nitric oxide, sepsis, and arginine metabolism. J Parenter Enteral Nutr 19:234–238
  Article CAS Google Scholar
• Kim SW, Wu G (2004) Dietary arginine supplementation enhances the growth of milk-fed young pigs. J Nutr 134:625–630
  PubMed CAS Google Scholar
• Kips JC (2001) Cytokines in asthma. Eur Respiratory J 18:24s–33s
  Article CAS Google Scholar
• Kong XF, Wu GY, Liao YP, Hou ZP, Liu HJ, Yin FG, Li TJ, Huang RL, Zhang YM, Deng D, Xie MY, Kang P, Yang CB, Yin YL, Fan MZ (2007) Dietary supplementation with Chinese herbal ultra-fine powder enhances cellular and humoral immunity in early-weaned piglet_s_. Livest Sci 108:94–98
  Article Google Scholar
• Kwak H, Austic RE, Dietert RR (1999) Influence of dietary arginine concentration on lymphoid organ growth in chickens. Poult Sci 78:1536–1541
  PubMed CAS Google Scholar
• Lalles JP, Bosi P, Smidt H, Stokes CR (2007) Weaning—a challenge to gut physiologists. Livest Sci 108:82–93
  Article Google Scholar
• Li P, Yin YL, Li DF, Kim SW, Wu G (2007) Amino acids and immune function. Br J Nutr 98:237–252
  Article PubMed CAS Google Scholar
• Ma CS, Nichols KE, Tangye SG (2007) Regulation of cellular and humoral immune responses by the SLAM and SAP families of molecules. Annu Rev Immunol 25:337–379
  Article PubMed CAS Google Scholar
• Mateo RD, Wu G, Bazer FW, Park JC, Shinzato I, Kim SW (2007) Dietary L-arginine supplementation enhances the reproductive performance of gilts. J Nutr 137:652–656
  PubMed CAS Google Scholar
• Montanez R, Sanchez-Jimenez F, Aldana-Montes JF, Medina MA (2007) Polyamines: metaboolism to systems biology and beyond. Amino Acids 33:283–289
  Article PubMed CAS Google Scholar
• Morris SM Jr (2002) Regulation of enzymes of the urea cycle and arginine metabolism. Annu Rev Nutr 22:87–105
  Article PubMed CAS Google Scholar
• National Research Council (NRC) (1998) Nutrient requirements of swine. National Academy Press, Washington, DC
  Google Scholar
• Nikolic J, Stojanovic I, Pavlovic R, Sokolovic D, Bjelakovic G, Beninati S (2007) The role of l-arginine in toxic liver failure: interrelation of arginase, polyamine catabolic enzymes and nitric oxide synrhase. Amino Acids 32:127–131
  Article PubMed CAS Google Scholar
• Ou DY, Li DF, Cao YH, Li XL, Yin JD, Qiao SY, Wu G (2007) Dietary supplementation with zinc oxide decreases expression of the stem cell factor in the small intestine of weanling pigs. J Nutr Biochem 18:820–826
  Article PubMed CAS Google Scholar
• Popovic PJ, Zeh HJ, Ochoa JB (2007) Arginine and immunity. J Nutr 136:1681S–1686S
  Google Scholar
• Reynolds JV, Daly JM, Shou J, Sigal R, Ziegler MM, Naji A (1990) Immunologic effects of arginine supplementation in tumor-bearing and non-tumor-bearing hosts. Ann Surg 211:202–210
  Article PubMed CAS Google Scholar
• Rodriguez PC, Zea AH, DeSalvo J, Culotta KS, Zabaleta J, Quiceno DG, Ochoa JB, Ochoa AC (2003) l-Arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J Immunol 171:1232–1239
  PubMed CAS Google Scholar
• Song M, Kellum JA (2005) Interleukin-6. Crit Care Med 33:463s–465s
  Article Google Scholar
• Wu G (1997) Synthesis of citrulline and arginine from proline in enterocytes of postnatal pigs. Am J Physiol Gastrointest Liver Physiol 272:G1382–G1390
  CAS Google Scholar
• Wu G, Bazer FW, Datta S, Johnson GA, Li P, Satterfield MC, Spencer TE (2008) Proline metabolism in the conceptus: Implications for fetal growth and development. Amino Acids. doi: 10.1007/s00726-008-0052-7
• Wu G, Bazer FW, Davis TA, Jaeger LA, Johnson GA, Kim SW, Knabe DA, Meininger CJ, Spencer TE, Yin YL (2007) Important roles for the arginine family of amino acids in swine nutrition and production. Livest Sci 112:8–22
  Article Google Scholar
• Wu G, Flynn NE, Knabe DA, Jaeger LA (2000) A cortisol surge mediates the enhanced polyamine synthesis in porcine enterocytes during weaning. Am J Physiol Regul Integr Comp Physiol 279:R554–R559
  PubMed CAS Google Scholar
• Wu G, Meier SA, Knabe DA (1996) Dietary glutamine supplementation prevents jejunal atrophy in weaned pigs. J Nutr 126:2578–2584
  PubMed CAS Google Scholar
• Wu G, Meininger CJ (2002) Regulation of nitric oxide synthesis by dietary factors. Annu Rev Nutr 22:61–86
  Article PubMed CAS Google Scholar
• Wu G, Ott TL, Knabe DA, Bazer FW (1999) Amino acid composition of the fetal pig. J Nutr 129:1031–1038
  PubMed CAS Google Scholar
• Wu G, Knabe DA, Kim SW (2004) Arginine: nutrition in neonatal pigs. J Nutr 134:2783S–2790S
  PubMed CAS Google Scholar
• Wu G, Morris SM Jr (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336:1–17
  PubMed CAS Google Scholar
• Zhan ZF, Ou DY, Piao XS, Kim SW, Liu YH, Wang JJ (2008) Dietary arginine supplementation affects microvascular development in the small intestine of early-weaned pigs. J Nutr 138:1304–1309
  PubMed CAS Google Scholar
• Yang WC, Schultz RD (1986) Ontogeny of natural killer cell activity and antibody dependent cell-mediated cytotoxicity in pigs. Dev Comp Immunol 10:405–418
  Article PubMed CAS Google Scholar
• Yao K, Yin YL, Chu WY, Liu ZQ, Deng D, Li TJ, Huang RL, Zhang JS, Tan BE, Wang W, Wu G (2008) Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. J Nutr 138:867–872
  PubMed CAS Google Scholar
• Yeh CL, Yeh SL, Lin MT, Chen WJ (2002) Effects of arginine-enriched total parenteral nutrition on inflammatory-related mediator and T-cell population in septic rats. Nutrition 18:631–635
  Article PubMed CAS Google Scholar

Download references

Acknowledgments

This research was supported by the Outstanding Overseas Chinese Scholars Fund of Chinese Academy of Sciences (CAS; no. 2005-1-4 and 2005-1-7), CAS Knowledge Innovation Project (no. YW-N-022 and KSCX2-SW-323), the National Basic Research Program of China (no. 2004CB117502), National Natural Science Foundation of China (no. 30671517, 30528006 and 30371038), Texas AgriLife Research (H-8200), and National Research Initiative Competitive Grant (no. 2008-35206-18764) from the USDA Cooperative State Research, Education, and Extension Service.

Author information

Authors and Affiliations

1. Laboratory of Animal Nutrition and Health, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, 410125, Changsha, Hunan, China
   Bie Tan, Xinguo G. Li, Xiangfeng Kong, Ruilin Huang, Kang Yao, Yulong Yin & Guoyao Wu
2. The Graduate School of the Chinese Academy of Sciences, 100039, Beijing, China
   Bie Tan & Kang Yao
3. Department of Animal Science, Texas A&M University, 2471 TAMU, College Station, TX, 77845, USA
   Bie Tan, Xiangfeng Kong & Guoyao Wu
4. Hunan Institute of Animal Husbandry and Veterinary Medicine, 410131, Changsha, Hunan, China
   Xinguo G. Li
5. Key Laboratory of Food Science of The Ministry of Education, Department of Food Science and Engineering, Nanchang University, 330047, Nanchang, China
   Zheng Ruan, Zeyuan Deng, Mingyong Xie & Yulong Yin
6. Department of Animal Nutrition, Ajinomoto Inc, Tokyo, 104-8135, Japan
   Izuru Shinzato

Authors

1. Bie Tan
   You can also search for this author inPubMed Google Scholar
2. Xinguo G. Li
   You can also search for this author inPubMed Google Scholar
3. Xiangfeng Kong
   You can also search for this author inPubMed Google Scholar
4. Ruilin Huang
   You can also search for this author inPubMed Google Scholar
5. Zheng Ruan
   You can also search for this author inPubMed Google Scholar
6. Kang Yao
   You can also search for this author inPubMed Google Scholar
7. Zeyuan Deng
   You can also search for this author inPubMed Google Scholar
8. Mingyong Xie
   You can also search for this author inPubMed Google Scholar
9. Izuru Shinzato
   You can also search for this author inPubMed Google Scholar
10. Yulong Yin
    You can also search for this author inPubMed Google Scholar
11. Guoyao Wu
    You can also search for this author inPubMed Google Scholar

Corresponding authors

Correspondence toYulong Yin or Guoyao Wu.

Rights and permissions

About this article

Cite this article

Tan, B., Li, X.G., Kong, X. et al. Dietary l-arginine supplementation enhances the immune status in early-weaned piglets.Amino Acids 37, 323–331 (2009). https://doi.org/10.1007/s00726-008-0155-1

Download citation

• Received: 21 April 2008
• Accepted: 02 July 2008
• Published: 19 August 2008
• Issue Date: July 2009
• DOI: https://doi.org/10.1007/s00726-008-0155-1

Keywords