Impact of viral disease hypophagia on pig jejunal function and integrity
Autoři:
Emma T. Helm aff001; Shelby M. Curry aff001; Carson M. De Mille aff001; Wesley P. Schweer aff001; Eric R. Burrough aff002; Nicholas K. Gabler aff001
Působiště autorů:
Department of Animal Science, Iowa State University, Ames, Iowa, United States of America
aff001; Department of Veterinary Diagnostic and Production Animal Medicine, Iowa State University, Ames, Iowa, United States of America
aff002
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0227265
Souhrn
Pathogen challenges are often accompanied by reductions in feed intake, making it difficult to differentiate impacts of reduced feed intake from impacts of pathogen on various response parameters. Therefore, the objective of this study was to determine the impact of Porcine Reproductive and Respiratory Syndrome virus (PRRSV) and feed intake on parameters of jejunal function and integrity in growing pigs. Twenty-four pigs (11.34 ± 1.54 kg BW) were randomly selected and allotted to 1 of 3 treatments (n = 8 pigs/treatment): 1) PRRSV naïve, ad libitum fed (Ad), 2) PRRSV-inoculated, ad libitum fed (PRRS+), and 3) PRRSV naïve, pair-fed to the PRRS+ pigs’ daily feed intake (PF). At 17 days post inoculation, all pigs were euthanized and the jejunum was collected for analysis. At days post inoculation 17, PRRS+ and PF pigs had decreased (P < 0.05) transepithelial resistance compared with Ad pigs; whereas fluorescein isothiocyanate-dextran 4 kDa permeability was not different among treatments. Active glucose transport was increased (P < 0.05) in PRRS+ and PF pigs compared with Ad pigs. Brush border carbohydrase activity was reduced in PRRS+ pigs compared with PF pigs for lactase (55%; P = 0.015), sucrase (37%; P = 0.002), and maltase (30%; P = 0.015). For all three carbohydrases, Ad pigs had activities intermediate that of PRRS+ and PF pigs. The mRNA abundance of the tight junction proteins claudin 2, claudin 3, claudin 4, occludin, and zonula occludens-1 were reduced in PRRS+ pigs compared with Ad pigs; however, neither the total protein abundance nor the cellular compartmentalization of these tight junction proteins differed among treatments. Taken together, this study demonstrates that the changes that occur to intestinal epithelium structure, function, and integrity during a systemic PRRSV challenge can be partially explained by reductions in feed intake. Further, long term adaptation to PRRSV challenge and caloric restriction does reduce intestinal transepithelial resistance but does not appear to reduce the integrity of tight junction protein complexes.
Klíčová slova:
Gastrointestinal tract – Glucose – Jejunum – Euthanasia – Nutrients – Swine – Tight junctions – Protein abundance
Zdroje
1. Adewole DI, Kim IH, Nyachoti CM. Gut Health of Pigs: Challenge Models and Response Criteria with a Critical Analysis of the Effectiveness of Selected Feed Additives—A Review. Asian-Australas J Anim Sci. 2016;29(7):909–24. doi: 10.5713/ajas.15.0795 26954144
2. Shen L, Weber CR, Raleigh DR, Yu D, Turner JR. Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol. 2011;73:283–309. doi: 10.1146/annurev-physiol-012110-142150 20936941
3. Pearce SC, Mani V, Boddicker RL, Johnson JS, Weber TE, Ross JW, et al. Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One. 2013;8(8):e70215. doi: 10.1371/journal.pone.0070215 23936392
4. Pearce SC, Mani V, Weber TE, Rhoads RP, Patience JF, Baumgard LH, et al. Heat stress and reduced plane of nutrition decreases intestinal integrity and function in pigs. J Anim Sci. 2013;91(11):5183–93. doi: 10.2527/jas.2013-6759 23989867
5. Moeser AJ, Pohl CS, Rajput M. Weaning stress and gastrointestinal barrier development: Implications for lifelong gut health in pigs. Anim Nutr. 2017;3(4):313–21. doi: 10.1016/j.aninu.2017.06.003 29767141
6. Boudry G, Lalles JP, Malbert CH, Bobillier E, Seve B. Diet-related adaptation of the small intestine at weaning in pigs is functional rather than structural. J Pediatr Gastroenterol Nutr. 2002;34(2):180–7. doi: 10.1097/00005176-200202000-00014 11840037
7. Curry SM, Schwartz KJ, Yoon KJ, Gabler NK, Burrough ER. Effects of porcine epidemic diarrhea virus infection on nursery pig intestinal function and barrier integrity. Vet Microbiol. 2017;211:58–66. doi: 10.1016/j.vetmic.2017.09.021 29102122
8. Schweer W, Pearce S, Burrough E, Schwartz K, Yoon K, Sparks J, et al. The effect of porcine reproductive and respiratory syndrome virus and porcine epidemic diarrhea virus challenge on growing pigs II: Intestinal integrity and function. Journal of Animal Science. 2016;94(2):523–32. doi: 10.2527/jas.2015-9836 27065122
9. Jung K, Ahn K, Chae C. Decreased activity of brush border membrane-bound digestive enzymes in small intestines from pigs experimentally infected with porcine epidemic diarrhea virus. Res Vet Sci. 2006;81(3):310–5. doi: 10.1016/j.rvsc.2006.03.005 16759679
10. Wiren M, Soderholm JD, Lindgren J, Olaison G, Permert J, Yang H, et al. Effects of starvation and bowel resection on paracellular permeability in rat small-bowel mucosa in vitro. Scand J Gastroenterol. 1999;34(2):156–62. doi: 10.1080/00365529950173014 10192193
11. Nunez MC, Bueno JD, Ayudarte MV, Almendros A, Rios A, Suarez MD, et al. Dietary restriction induces biochemical and morphometric changes in the small intestine of nursing piglets. J Nutr. 1996;126(4):933–44. doi: 10.1093/jn/126.4.933 8613897
12. Habold C, Chevalier C, Dunel-Erb S, Foltzer-Jourdainne C, Le Maho Y, Lignot JH. Effects of fasting and refeeding on jejunal morphology and cellular activity in rats in relation to depletion of body stores. Scand J Gastroenterol. 2004;39(6):531–9. doi: 10.1080/00365520410004514 15223676
13. Johnson RW. The concept of sickness behavior: a brief chronological account of four key discoveries. Vet Immunol Immunopathol. 2002;87(3–4):443–50. doi: 10.1016/s0165-2427(02)00069-7 12072271
14. Plata-Salaman CR. Anorexia during acute and chronic disease. Nutrition. 1996;12(2):69–78. doi: 10.1016/s0899-9007(96)90702-9 8724375
15. Adamo SA. Parasitic suppression of feeding in the tobacco hornworm, Manduca sexta: parallels with feeding depression after an immune challenge. Arch Insect Biochem Physiol. 2005;60(4):185–97. doi: 10.1002/arch.20068 16304613
16. Helm ET, Curry SM, De Mille CM, Schweer WP, Burrough ER, Zuber EA, et al. Impact of porcine reproductive and respiratory syndrome virus on muscle metabolism of growing pigs1. J Anim Sci. 2019;97(8):3213–27. doi: 10.1093/jas/skz168 31212312
17. Curry SM, Gibson KA, Burrough ER, Schwartz KJ, Yoon KJ, Gabler NK. Nursery pig growth performance and tissue accretion modulation due to porcine epidemic diarrhea virus or porcine deltacoronavirus challenge. J Anim Sci. 2017;95(1):173–81. doi: 10.2527/jas.2016.1000 28177368
18. Schweer WP, Schwartz K, Burrough ER, Yoon KJ, Sparks JC, Gabler NK. The effect of porcine reproductive and respiratory syndrome virus and porcine epidemic diarrhea virus challenge on growing pigs I: Growth performance and digestibility. J Anim Sci. 2016;94(2):514–22. doi: 10.2527/jas.2015-9834 27065121
19. Helm ET, Outhouse AC, Schwartz KJ, Lonergan SM, Curry SM, Dekkers JCM, et al. Metabolic adaptation of pigs to a Mycoplasma hyopneumoniae and Lawsonia intracellularis dual challenge. J Anim Sci. 2018;96(8):3196–207. doi: 10.1093/jas/sky220 29860328
20. van der Wolf PJ, Wientjes JGM, Heuvelink AE, Veldhuis AMB, van Hees HMJ, Roubos-van den Hil PJ. Development of a Salmonella Typhimurium challenge model in weaned pigs to evaluate effects of water and feed interventions on fecal shedding and growth performance. J Anim Sci. 2017;95(7):2879–90. doi: 10.2527/jas.2016.1136 28727108
21. Li Q, Burrough ER, Gabler NK, Loving CL, Sahin O, Gould SA, et al. A soluble and highly fermentable dietary fiber with carbohydrases improved gut barrier integrity markers and growth performance in F18 ETEC challenged pigs1. J Anim Sci. 2019;97(5):2139–53. doi: 10.1093/jas/skz093 30888017
22. Nathues H, Alarcon P, Rushton J, Jolie R, Fiebig K, Jimenez M, et al. Cost of porcine reproductive and respiratory syndrome virus at individual farm level—An economic disease model. Prev Vet Med. 2017;142:16–29. doi: 10.1016/j.prevetmed.2017.04.006 28606362
23. Schweer W, Schwartz K, Patience JF, Karriker L, Sparks C, Weaver M, et al. Porcine Reproductive and Respiratory Syndrome virus reduces feed efficiency, digestibility, and lean tissue accretion in grow-finish pigs. Transl Anim Sci. 2017. doi: 10.2527/tas2016.0008
24. Lochmiller RL, Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos. 2000;88(1):87–98. doi: 10.1034/j.1600-0706.2000.880110.x
25. O'Neill LA, Pearce EJ. Immunometabolism governs dendritic cell and macrophage function. J Exp Med. 2016;213(1):15–23. doi: 10.1084/jem.20151570 26694970
26. Ganeshan K, Chawla A. Metabolic regulation of immune responses. Annu Rev Immunol. 2014;32(1):609–34. doi: 10.1146/annurev-immunol-032713-120236 24655299
27. Rolfe DF, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev. 1997;77(3):731–58. doi: 10.1152/physrev.1997.77.3.731 9234964
28. Helm ET, Curry SM, De Mille CM, Schweer WP, Burrough ER, Zuber EA, et al. Impact of porcine reproductive and respiratory syndrome virus on muscle metabolism of growing pigs. J Anim Sci. 2019;97(8):3213–27. doi: 10.1093/jas/skz168 31212312
29. Klinge KL, Vaughn EM, Roof MB, Bautista EM, Murtaugh MP. Age-dependent resistance to Porcine reproductive and respiratory syndrome virus replication in swine. Virol J. 2009;6:177. doi: 10.1186/1743-422X-6-177 19860914
30. Helm ET, Curry S, Trachsel JM, Schroyen M, Gabler NK. Evaluating nursery pig responses to in-feed sub-therapeutic antibiotics. PLoS One. 2019;14(4):e0216070. doi: 10.1371/journal.pone.0216070 31026263
31. Ueda I, Wada T. Determination of inorganic phosphate by the molybdovanadate method in the presence of ATP and some interfering organic bases. Anal Biochem. 1970;37:169–74. doi: 10.1016/0003-2697(70)90273-3 4394190
32. Dahlqvist A. Assay of intestinal disaccharidases. Scand J Clin Lab Invest. 1984;44(2):169–72. doi: 10.3109/00365518409161400 6719024
33. Roncari G, Zuber H. Thermophilic aminopeptidases from Bacillus stearothermophilus. I. Isolation, specificity, and general properties of the thermostable aminopeptidase I. Int J Protein Res. 1969;1(1):45–61. doi: 10.1111/j.1399-3011.1969.tb01625.x 5001155
34. Rochell SJ, Alexander LS, Rocha GC, Van Alstine WG, Boyd RD, Pettigrew JE, et al. Effects of dietary soybean meal concentration on growth and immune response of pigs infected with porcine reproductive and respiratory syndrome virus. J Anim Sci. 2015;93(6):2987–97. doi: 10.2527/jas.2014-8462 26115285
35. Toepfer-Berg TL, Escobar J, Van Alstine WG, Baker DH, Salak-Johnson J, Johnson RW. Vitamin E supplementation does not mitigate the acute morbidity effects of porcine reproductive and respiratory syndrome virus in nursery pigs. J Anim Sci. 2004;82(7):1942–51. doi: 10.2527/2004.8271942x 15309940
36. Escobar J, Toepfer-Berg TL, Chen J, Van Alstine WG, Campbell JM, Johnson RW. Supplementing drinking water with Solutein did not mitigate acute morbidity effects of porcine reproductive and respiratory syndrome virus in nursery pigs. J Anim Sci. 2006;84(8):2101–9. doi: 10.2527/jas.2005-616 16864870
37. Murtaugh MP, Xiao Z, Zuckermann F. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunol. 2002;15(4):533–47. doi: 10.1089/088282402320914485 12513925
38. National Research Council. Nutrient requirements of swine: Eleventh revised edition. Washington, DC: The National Academies Press; 2012.
39. Brown HO, Levine ML, Lipkin M. Inhibition of intestinal epithelial cell renewal and migration induced by starvation. Am J Physiol. 1963;205(5):868–72. doi: 10.1152/ajplegacy.1963.205.5.868 5877415
40. Schweer WP, Pearce SC, Burrough ER, Schwartz K, Yoon KJ, Sparks JC, et al. The effect of porcine reproductive and respiratory syndrome virus and porcine epidemic diarrhea virus challenge on growing pigs II: Intestinal integrity and function. J Anim Sci. 2016;94(2):523–32. doi: 10.2527/jas.2015-9836 27065122
41. Drozdowski LA, Thomson AB. Intestinal sugar transport. World J Gastroenterol. 2006;12(11):1657–70. doi: 10.3748/wjg.v12.i11.1657 16586532
42. Helm ET, Curry SM, Schwartz KJ, Lonergan SM, Gabler NK. Mycoplasma hyopneumoniae-Lawsonia intracellularis dual challenge modulates intestinal integrity and function1. J Anim Sci. 2019;97(6):2376–84. doi: 10.1093/jas/skz112 30980078
43. Rakhshandeh A, Dekkers JC, Kerr BJ, Weber TE, English J, Gabler NK. Effect of immune system stimulation and divergent selection for residual feed intake on digestive capacity of the small intestine in growing pigs. J Anim Sci. 2012;90 Suppl 4(Supplement_4):233–5. doi: 10.2527/jas.53976 23365340
44. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, et al. Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature. 2013;496(7444):238–42. doi: 10.1038/nature11986 23535595
45. O'Neill LA, Kishton RJ, Rathmell J. A guide to immunometabolism for immunologists. Nat Rev Immunol. 2016;16(9):553–65. doi: 10.1038/nri.2016.70 27396447
46. Binder HJaAR. Nutrient digestion and absorption. In: Boron WFaELB, editor. Medical physiology: a cellular and molecular approach. 2nd ed. Philadelphia, PA: Saunders Elsevier; 2012. p. 949–79.
47. Barreau F, Hugot JP. Intestinal barrier dysfunction triggered by invasive bacteria. Curr Opin Microbiol. 2014;17:91–8. doi: 10.1016/j.mib.2013.12.003 24440560
48. Jung K, Saif LJ. Goblet cell depletion in small intestinal villous and crypt epithelium of conventional nursing and weaned pigs infected with porcine epidemic diarrhea virus. Res Vet Sci. 2017;110:12–5. doi: 10.1016/j.rvsc.2016.10.009 28159230
49. Lu Z, Ding L, Lu Q, Chen YH. Claudins in intestines: Distribution and functional significance in health and diseases. Tissue Barriers. 2013;1(3):e24978. doi: 10.4161/tisb.24978 24478939
50. Pearce SC, Sanz-Fernandez MV, Hollis JH, Baumgard LH, Gabler NK. Short-term exposure to heat stress attenuates appetite and intestinal integrity in growing pigs. J Anim Sci. 2014;92(12):5444–54. doi: 10.2527/jas.2014-8407 25367514
51. Jacobi SK, Moeser AJ, Blikslager AT, Rhoads JM, Corl BA, Harrell RJ, et al. Acute effects of rotavirus and malnutrition on intestinal barrier function in neonatal piglets. World J Gastroenterol. 2013;19(31):5094–102. doi: 10.3748/wjg.v19.i31.5094 23964143
52. Garas LC, Feltrin C, Hamilton MK, Hagey JV, Murray JD, Bertolini LR, et al. Milk with and without lactoferrin can influence intestinal damage in a pig model of malnutrition. Food Funct. 2016;7(2):665–78. doi: 10.1039/c5fo01217a 26751615
53. Garas LC, Hamilton MK, Dawson MW, Wang J-L, Murray JD, Raybould HE, et al. Lysozyme-rich milk mitigates effects of malnutrition in a pig model of malnutrition and infection. Br J Nutr. 2018;120(10):1131–48. doi: 10.1017/S0007114518002507 30400999
54. van Goudoever JB, Stoll B, Henry JF, Burrin DG, Reeds PJ. Adaptive regulation of intestinal lysine metabolism. Proc Natl Acad Sci U S A. 2000;97(21):11620–5. doi: 10.1073/pnas.200371497 11016965
55. Hou Y, Yao K, Wang L, Ding B, Fu D, Liu Y, et al. Effects of alpha-ketoglutarate on energy status in the intestinal mucosa of weaned piglets chronically challenged with lipopolysaccharide. Br J Nutr. 2011;106(3):357–63. doi: 10.1017/S0007114511000249 21342606
56. Scharl M, Paul G, Barrett KE, McCole DF. AMP-activated protein kinase mediates the interferon-gamma-induced decrease in intestinal epithelial barrier function. J Biol Chem. 2009;284(41):27952–63. doi: 10.1074/jbc.M109.046292 19654324
57. VanItallie CM, Anderson JM. Occludin confers adhesiveness when expressed in fibroblasts. J Cell Sci. 1997;110:1113–21. 9175707
58. Furuse M, Sasaki H, Fujimoto K, Tsukita S. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol. 1998;143(2):391–401. doi: 10.1083/jcb.143.2.391 9786950
59. Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, Hopkins AM, et al. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol. 2003;171(11):6164–72. doi: 10.4049/jimmunol.171.11.6164 14634132
60. Ueno PM, Oriá RB, Maier EA, Guedes M, de Azevedo OG, Wu D, et al. Alanyl-glutamine promotes intestinal epithelial cell homeostasis in vitro and in a murine model of weanling undernutrition. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2011;301(4):G612–G22. doi: 10.1152/ajpgi.00531.2010 21799183
61. Brown DR. Catecholamine-Directed Epithelial Cell Interactions with Bacteria in the Intestinal Mucosa. Adv Exp Med Biol. 2016;874:79–99. doi: 10.1007/978-3-319-20215-0_3 26589214
62. Harvald EB, Sprenger RR, Dall KB, Ejsing CS, Nielsen R, Mandrup S, et al. Multi-omics Analyses of Starvation Responses Reveal a Central Role for Lipoprotein Metabolism in Acute Starvation Survival in C. elegans. Cell systems. 2017;5(1):38–52. e4. doi: 10.1016/j.cels.2017.06.004 28734827
Článok vyšiel v časopise
PLOS One
2020 Číslo 1
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Masturbační chování žen v ČR − dotazníková studie
- Nejasný stín na plicích – kazuistika
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Metformin zlepšuje u žen se syndromem polycystických ovarií pravidelnost menstruačního cyklu i hormonální a metabolický profil
Najčítanejšie v tomto čísle
- Psychometric validation of Czech version of the Sport Motivation Scale
- Comparison of Monocyte Distribution Width (MDW) and Procalcitonin for early recognition of sepsis
- Effects of supplemental creatine and guanidinoacetic acid on spatial memory and the brain of weaned Yucatan miniature pigs
- Accelerated sparsity based reconstruction of compressively sensed multichannel EEG signals