Skip to main content

Development and Renewal of Intestinal Villi in Pigs

  • Chapter
  • First Online:
Nutritional and Physiological Functions of Amino Acids in Pigs

Abstract

The gastrointestinal mucosa of pig not only acts as an organ for diet digestion and absorption but also plays an important role in fighting against pathogenic bacteria and toxic substances presented in intestinal lumen. The development of gastrointestinal mucosa begins in the early embryo and self-renews during the whole life. Its homeostasis is preserved via regulating the proliferation, growth arrest, differentiation, and apoptosis of epithelial cell. Moreover, the developmental and renewal processes of gastrointestinal mucosa are regulated by various factors, such as genetic, neural, hormonal and dietary influences and disturbed by weaning stress. Pig gastrointestinal mucosa is not a very common experimental model, and therefore, some information discussed in this chapter is obtained from other species.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

HNF-1α:

Hepatocyte nuclear factor-1α

Cdx1:

Caudal-related homeobox protein 1

Cdx2:

Caudal-related homeobox protein 2

VFE:

Vacuolated fetal-type enterocytes

SEM:

Scanning electron microscopy

CVA:

Crypt–villus axis

TCF:

T-cell factor

BMP:

Bone morphogenetic protein

TGF-β:

Transforming growth factor beta

GATA 4:

GATA-binding transcription factor 4

GATA 5:

GATA-binding transcription factor 5

GATA 6:

GATA-binding transcription factor 6

HES1:

Hairy/enhancer of split homolog 1

Atoh1:

Atonal homolog 1

EAAC1:

Excitatory amino acid carrier 1

SGLT1:

Sodium/glucose cotransporter 1

SLC6A19:

Solute carrier family 6, member 19

ASCT2:

Alanine-serine-cysteine transporter 2

PP:

Polish landrace/Pietrain

DHW:

Duroc/Hampshire/wild boar

GLUT5:

Glucose transporter member 5

ENS:

Enteric nervous systems

IGF-I:

Insulin-like growth factor I

IGF-II:

Insulin-like growth factor II

EGF:

Epidermal growth factor

References

  • Amerongen HM, Mack JA, Wilson JM, Neutra MR (1989) Membrane domains of intestinal epithelial cells: distribution of Na+, K+-ATPase and the membrane skeleton in adult rat intestine during fetal development and after epithelial isolation. J Cell Biol 109:2129–2138

    Article  PubMed  CAS  Google Scholar 

  • Batts LE, Polk DB, Dubois RN, Kulessa H (2006) Bmp signaling is required for intestinal growth and morphogenesis. Dev Dyn 235:1563–1570

    Article  PubMed  CAS  Google Scholar 

  • Ben Lulu S, Coran AG, Mogilner JG, Shaoul R, Shamir R, Shehadeh N, Sukhotnik I (2010) Oral insulin stimulates intestinal epithelial cell turnover in correlation with insulin-receptor expression along the villus-crypt axis in a rat model of short bowel syndrome. Pediatr Surg Int 26:37–44

    Article  PubMed  Google Scholar 

  • Boudreau F, Rings EH, van Wering HM, Kim RK, Swain GP, Krasinski SD, Moffett J, Grand RJ, Suh ER, Traber PG (2002) Hepatocyte nuclear factor-1α, GATA-4, and caudal related homeodomain protein Cdx2 interact functionally to modulate intestinal gene transcription. J Biol Chem 277:31909–31917

    Article  PubMed  CAS  Google Scholar 

  • Boudry G, Péron V, Le Huërou-Luron I, Lallès JP, Sève B (2004) Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. J Nutr 134:2256–2262

    PubMed  CAS  Google Scholar 

  • Buchmiller TL, Fonkalsrud EW, Kim CS, Chopourian HL, Shaw KS, Lam MM, Diamond JM (1992) Upregulation of nutrient transport in fetal rabbit intestine by transamniotic substrate administration. J Surg Res 52:443–447

    Article  PubMed  CAS  Google Scholar 

  • Buddington RK (1992) Intestinal nutrient transport during ontogeny of vertebrates. Am J Physiol 263:R503–R509

    PubMed  CAS  Google Scholar 

  • Buddington RK (1994) Nutrition and ontogenetic development of the intestine. Can J Physiol Pharmacol 72:251–259

    Article  PubMed  CAS  Google Scholar 

  • Burgess AW (1998) Growth control mechanisms in normal and transformed intestinal cells. Philos Trans R Soc Lond B Biol Sci 353:903–909

    Article  PubMed  CAS  Google Scholar 

  • Burns AJ, Roberts RR, Bornstein JC, Young HM (2009) Development of the enteric nervous system and its role in intestinal motility during fetal and early postnatal stages. Semin Pediatr Surg 18:196–205

    Article  PubMed  Google Scholar 

  • Burrin DG, Stoll B, Guan X, Cui L, Chang X, Holst JJ (2005) Glucagon-like peptide 2 dose-dependently activates intestinal cell survival and proliferation in neonatal piglets. Endocrinology 146:22–32

    Article  PubMed  CAS  Google Scholar 

  • Burrin DG, Wester TJ, Davis TA, Amick S, Heath JP (1996) Orally administered IGF-I increases intestinal mucosal growth in formula-fed neonatal pigs. Am J Physiol 270:R1085–R1091

    PubMed  CAS  Google Scholar 

  • Burzynski G, Shepherd IT, Enomoto H (2009) Genetic model system studies of the development of the enteric nervous system, gut motility and Hirschsprung’s disease. Neurogastroenterol Motil 21:113–127

    Article  PubMed  CAS  Google Scholar 

  • Buts JP, De Keyser N, Kolanowski J, Sokal E, Van Hoof F (1993) Maturation of villus and crypt cell functions in rat small intestine. Role of dietary polyamines. Dig Dis Sci 38:1091–1098

    Article  PubMed  CAS  Google Scholar 

  • Buts JP, De Keyser N, Marandi S, Maernoudt AS, Sokal EM, Rahier J, Hermans D (1997) Expression of insulin receptors and of 60-kDa receptor substrate in rat mature and immature enterocytes. Am J Physiol 273:G217–G226

    PubMed  CAS  Google Scholar 

  • Cera KR, Mahan DC, Cross RF, Reinhart GA, Whitmoyer RE (1988) Effect of age, weaning and postweaning diet on small intestinal growth and jejunal morphology in young swine. J Anim Sci 66:574–584

    PubMed  CAS  Google Scholar 

  • Chang J, Chance MR, Nicholas C, Ahmed N, Guilmeau S, Flandez M, Wang D, Byun DS, Nasser S, Albanese JM, Corner GA, Heerdt BG, Wilson AJ, Augenlicht LH, Mariadason JM (2008) Proteomic changes during intestinal cell maturation in vivo. J Proteomics 71:530–546

    Article  PubMed  CAS  Google Scholar 

  • Chen K, Nezu R, Wasa M, Sando K, Kamata S, Takagi Y, Okada A (1999) Insulin-like growth factor-1 modulation of intestinal epithelial cell restitution. JPEN J Parenter Enteral Nutr 23:S89–S92

    Article  PubMed  CAS  Google Scholar 

  • Cheng H, Leblond CP (1974a) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine I. Columnar cell. Am J Anat 141:461–479

    Article  PubMed  CAS  Google Scholar 

  • Cheng H, Leblond CP (1974b) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine V. Unitarian theory of the origin of the four epithelial cell types. Am J Anat 141:537–561

    Article  PubMed  CAS  Google Scholar 

  • Clatworthy JP, Subramanian V (2001) Stem cells and the regulation of proliferation, differentiation and patterning in the intestinal epithelium: emerging insights from gene expression patterns, transgenic and gene ablation studies. Mech Dev 101:3–9

    Article  PubMed  CAS  Google Scholar 

  • Davidson NO, Hausman AM, Ifkovits CA, Buse JB, Gould GW, Burant CF, Bell GI (1992) Human intestinal glucose transporter expression and localization of GLUT5. Am J Physiol 262:C795–C800

    PubMed  CAS  Google Scholar 

  • Davis TA, Bush JA, Vann RC, Suryawan A, Kimball SR, Burrin DG (2004) Somatotropin regulation of protein metabolism in pigs. J Anim Sci 82(E-Suppl):E207–E213

    PubMed  Google Scholar 

  • Fan MZ, Matthews JC, Etienne NM, Stoll B, Lackeyram D, Burrin DG (2004) Expression of apical membrane l-glutamate transporters in neonatal porcine epithelial cells along the small intestinal crypt-villus axis. Am J Physiol Gastrointest Liver Physiol 287:G385–G398

    Article  PubMed  CAS  Google Scholar 

  • Fan MZ, Stoll B, Jiang R, Burrin DG (2001) Enterocyte digestive enzyme activity along the crypt-villus and longitudinal axes in the neonatal pig small intestine. J Anim Sci 79:371–381

    PubMed  CAS  Google Scholar 

  • Foltzer-Jourdainne C, Kedinger M, Raul F (1989) Perinatal expression of brush-border hydrolases in rat colon: hormonal and tissue regulations. Am J Physiol 257:G496–G503

    PubMed  CAS  Google Scholar 

  • Forstner JF (1978) Intestinal mucins in health and disease. Digestion 17:234–263

    Article  PubMed  CAS  Google Scholar 

  • Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123:1777–1788

    Article  PubMed  CAS  Google Scholar 

  • Gao X, Sedgwick T, Shi YB, Evans T (1998) Distinct functions are implicated for the GATA-4, -5, and -6 transcription factors in the regulation of intestine epithelial cell differentiation. Mol Cell Biol 18:2901–2911

    PubMed  CAS  Google Scholar 

  • Gordon JI, Hermiston ML (1994) Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr Opin Cell Biol 6:795–803

    Article  PubMed  CAS  Google Scholar 

  • Gu X, Li D, She R (2002) Effect of weaning on small intestinal structure and function in the piglet. Arch Tierernahr 56:275–286

    Article  PubMed  CAS  Google Scholar 

  • Hampson DJ (1986) Alterations in piglet small intestinal structure at weaning. Res Vet Sci 40:32–40

    PubMed  CAS  Google Scholar 

  • He XC, Zhang J, Tong WG, Tawfik O, Ross J, Scoville DH, Tian Q, Zeng X, He X, Wiedemann LM, Mishina Y, Li L (2004) BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet 36:1117–1121

    Article  PubMed  CAS  Google Scholar 

  • Henning SJ (1980) Postnatal development of jejunal sucrase: independence from cyclic AMP. Biol Neonate 37:246–253

    Article  PubMed  CAS  Google Scholar 

  • Henning SJ (1981) Postnatal development: coordination of feeding, digestion, and metabolism. Am J Physiol 241:G199–G214

    PubMed  CAS  Google Scholar 

  • Houle VM, Schroeder EA, Odle J, Donovan SM (1997) Small intestinal disaccharidase activity and ileal villus height are increased in piglets consuming formula containing recombinant human insulin-like growth factor-I. Pediatr Res 42:78–86

    Article  PubMed  CAS  Google Scholar 

  • Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S (1999) Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 147:1351–1363

    Article  PubMed  CAS  Google Scholar 

  • Jenness R, Sloan RE (1970) The composition of milks of various species: a review. Dairy Sci Abstr 32:599–612

    Google Scholar 

  • Karam SM (1999) Lineage commitment and maturation of epithelial cells in the gut. Front Biosci 4:D286–D298

    Article  PubMed  CAS  Google Scholar 

  • Kedinger M, Lefebvre O, Duluc I, Freund JN, Simon-Assmann P (1998) Cellular and molecular partners involved in gut morphogenesis and differentiation. Philos Trans R Soc Lond B Biol Sci 353:847–856

    Article  PubMed  CAS  Google Scholar 

  • Keen CL, Lönnerdal B, Clegg M, Hurley LS (1981) Developmental changes in composition of rat milk: trace elements, minerals, protein, carbohydrate and fat. J Nutr 111:226–236

    PubMed  CAS  Google Scholar 

  • Kelly D, Smyth JA, McCracken KJ (1991) Digestive development of the early-weaned pig. I. Effect on continuous nutrient supply on the development of the digestive tract and on changes in digestive enzyme activity during the first week post-weaning. Br J Nutr 65:169–180

    Article  PubMed  CAS  Google Scholar 

  • Kim JC, Hansen CF, Mullan BP, Pluske JR (2012) Nutrition and pathology of weaner pigs: nutritional strategies to support barrier function in the gastrointestinal tract. Anim Feed Sci Technol 173:3–16

    Article  CAS  Google Scholar 

  • Kong XF, Tan BE, Yin YL, Li XL, Jaeger LA, Bazer FW, Wu GY (2012b) Arginine stimulates the mTOR signaling pathway and protein synthesis in porcine trophectoderm cells. J Nutr Biochem 23(9):1178–1183

    Article  PubMed  CAS  Google Scholar 

  • Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H (1998) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19:379–383

    Article  PubMed  CAS  Google Scholar 

  • Kotunia A, Woliński J, Słupecka M, Dolman D, Kato I, Kuwahara A, Zabielski R (2006) Exogenous ghrelin retards the development of the small intestine in pig neonates fed with artificial milk formula. Book of abstracts, digestive physiology in pigs. 25–27 May 2006, Vejle, Denmark. pp 82

    Google Scholar 

  • Lacroix B, Kedinger M, Simon-Assmann P, Rousset M, Zweibaum A, Haffen K (1984) Developmental pattern of brush border enzymes in the human fetal colon. Correlation with some morphogenetic events. Early Hum Dev 9:95–103

    Article  PubMed  CAS  Google Scholar 

  • Le Dividich J, Seve B (2000) Effects of underfeeding during the weaning period on growth, metabolism and hormonal adjustments in the piglet. Dom Anim Endocrinol 19:63–74

    Article  Google Scholar 

  • Leeper LL, Henning SJ (1990) Development and tissue distribution of sucrase-isomaltase mRNA in rats. Am J Physiol 258:G52–G58

    PubMed  CAS  Google Scholar 

  • Lemmey AB, Martin AA, Read LC, Tomas FM, Owens PC, Ballard FJ (1991) IGF-I and the truncated analogue des-(1-3) IGF-I enhance growth in rats after gut resection. Am J Physiol 260:E213–E219

    PubMed  CAS  Google Scholar 

  • Liao Y, Lönnerdal B (2010) Global microRNA characterization reveals that miR-103 is involved in IGF-1 stimulated mouse intestinal cell proliferation. PLoS One 5(9):e12976

    Article  PubMed  Google Scholar 

  • Lund PK (1998) Molecular basis of intestinal adaptation: the role of the insulin-like growth factor system. Ann N Y Acad Sci 859:18–36

    Article  PubMed  CAS  Google Scholar 

  • Mariadason JM, Bordonaro M, Aslam F, Shi L, Kuraguchi M, Velcich A, Augenlicht LH (2001) Down-regulation of β-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Res 61:3465–3471

    PubMed  CAS  Google Scholar 

  • Mariadason JM, Nicholas C, L’Italien KE, Zhuang M, Smartt HJ, Heerdt BG, Yang W, Corner GA, Wilson AJ, Klampfer L, Arango D, Augenlicht LH (2005) Gene expression profiling of intestinal epithelial cell maturation along the crypt-villus axis. Gastroenterology 128:1081–1088

    Article  PubMed  CAS  Google Scholar 

  • Mathan M, Moxey PC, Trier JS (1976) Morphogenesis of fetal rat duodenal villi. Am J Anat 146:73–92

    Article  PubMed  CAS  Google Scholar 

  • Menard D, Calvert R (1991) Fetal and postnatal development of the small and large intestine: patterns and regulation. In: Morisset J, Solomon TE (eds) Growth of the gastrointestinal tract: gastrointestinal hormones and growth factors. CRC, Boca Raton, FL, pp 159–174

    Google Scholar 

  • Ménard D, Dagenais P, Calvert R (1994) Morphological changes and cellular proliferation in mouse colon during fetal and postnatal development. Anat Rec 238:349–359

    Article  PubMed  Google Scholar 

  • Mutoh H, Hakamata Y, Sato K, Eda A, Yanaka I, Honda S, Osawa H, Kaneko Y, Sugano K (2002) Conversion of gastric mucosa to intestinal metaplasia in Cdx2-expressing transgenic mice. Biochem Biophys Res Commun 294:470–479

    Article  PubMed  CAS  Google Scholar 

  • Nanthakumar NN, Henning SJ (1993) Ontogeny of sucrase-isomaltase gene expression in rat intestine: responsiveness to glucocorticoids. Am J Physiol 264:G306–G311

    PubMed  CAS  Google Scholar 

  • Nishimura S, Takahashi M, Ota S, Hirano M, Hiraishi H (1998) Hepatocyte growth factor accelerates restitution of intestinal epithelial cells. J Gastroenterol 33:172–178

    Article  PubMed  CAS  Google Scholar 

  • Ono K (1977) Absorption of horseradish peroxidase by the principal cells of the large intestines of postnatal developing rats. Anat Embryol (Berl) 151:53–62

    Article  CAS  Google Scholar 

  • Pácha J (2000) Development of intestinal transport function in mammals. Physiol Rev 80:1633–1667

    PubMed  Google Scholar 

  • Pluske JR, Hampson DJ, Williams IH (1997) Factors influencing the structure and function of the small intestine in weaned pig: a review. Livest Prod Sci 51:215–236

    Article  Google Scholar 

  • Raul F, Simon P, Kedinger M, Haffen K (1977) Intestinal enzymes activities in isolated villus and crypt cells during postnatal development of the rat. Cell Tissue Res 176:167–178

    Article  PubMed  CAS  Google Scholar 

  • Roth KA, Rubin DC, Birkenmeier EH, Gordon JI (1991) Expression of liver fatty acid-binding protein/human growth hormone fusion genes within the enterocyte and enteroendocrine cell populations of fetal transgenic mice. J Biol Chem 266:5949–5954

    PubMed  CAS  Google Scholar 

  • Rowling PJ, Sepúlveda FV (1984) The distribution of (Na+/K+)-ATPase along the villus crypt-axis in the rabbit small intestine. Biochim Biophys Acta 771:35–41

    Article  PubMed  CAS  Google Scholar 

  • Schmidt GH, Winton DJ, Ponder BA (1988) Development of the pattern of cell renewal in the crypt-villus unit of chimaeric mouse small intestine. Development 103:785–790

    PubMed  CAS  Google Scholar 

  • Shanahan F (1997) A gut reaction—lymphoepithelial communication in the intestine. Science 275:1897–1898

    Article  PubMed  CAS  Google Scholar 

  • Sheng G, Bernabe KQ, Guo J, Warner BW (2006) Epidermal growth factor receptor-mediated proliferation of enterocytes requires p21waf1/cip1 expression. Gastroenterology 131:153–164

    Article  PubMed  CAS  Google Scholar 

  • Shie JL, Chen ZY, O’Brien MJ, Pestell RG, Lee ME, Tseng CC (2000) Role of gut-enriched Kruppel-like factor in colonic cell growth and differentiation. Am J Physiol Gastrointest Liver Physiol 279:G806–G814

    PubMed  CAS  Google Scholar 

  • Shu R, David ES, Ferraris RP (1997) Dietary fructose enhances intestinal fructose transport and GLUT5 expression in weaning rats. Am J Physiol 272:G446–G453

    PubMed  CAS  Google Scholar 

  • Simon TC, Gordon JI (1995) Intestinal epithelial cell differentiation: new insights from mice, flies and nematodes. Curr Opin Genet Dev 5:577–586

    Article  PubMed  CAS  Google Scholar 

  • Skrzypek T, Valverde Piedra JL, Skrzypek H, Kazimierczak W, Biernat M, Zabielski R (2007a) Gradual disappearance of vacuolated enterocytes in the small intestine of neonatal piglets. J Physiol Pharmacol 58(Suppl 3):87–95

    PubMed  Google Scholar 

  • Skrzypek T, Valverde Piedrab JL, Skrzypeka H, Kazimierczaka W, Szymańczykb S, Pawłowskab M, Zabielskic R (2007b) Intestinal villi structure during the development of pig and wild boar crossbreed neonates. Livest Sci 109:38–41

    Article  Google Scholar 

  • Skrzypek T, Valverde Piedra JL, Skrzypek H, Woliński J, Kazimierczak W, Szymańczyk S, Pawłowska M, Zabielski R (2005) Light and scanning electron microscopy evaluation of the postnatal small intestinal mucosa development in pigs. J Physiol Pharmacol 56(Suppl 3):71–87

    PubMed  Google Scholar 

  • Skrzypek T, Valverde Piedrab JL, Skrzypeka H, Kazimierczaka W, Szymanczykb SE, Zabielskic R (2010) Changes in pig small intestinal absorptive area during the first 14 days. Livest Sci 133:53–56

    Article  Google Scholar 

  • Słupecka M, Woliński J, Zabielski R (2005) Leptin affects the p53 expression in the gut mucosa of neonatal piglets. Proceedings of the 13th Euro-conference on apoptosis, Budapest, Hungary, 2005 October 1–4, Abstract. pp 207.

    Google Scholar 

  • Smith MW (1985) Expression of digestive and absorptive function in differentiating enterocytes. Annu Rev Physiol 47:247–260

    Article  PubMed  CAS  Google Scholar 

  • Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA (1986) Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 103:755–766

    Article  PubMed  CAS  Google Scholar 

  • Subramoniam A (1979) Rat small intestinal morphology with special reference to villi: effects of maternal protein deficiency and hydrocortisone. Acta Anat (Basel) 104:439–450

    Article  CAS  Google Scholar 

  • Toloza EM, Diamond J (1992) Ontogenetic development of nutrient transporters in rat intestine. Am J Physiol 263:G593–G604

    PubMed  CAS  Google Scholar 

  • Traber PG, Gumucio DL, Wang W (1991) Isolation of intestinal epithelial cells for the study of differential gene expression along the crypt-villus axis. Am J Physiol 260:G895–G903

    PubMed  CAS  Google Scholar 

  • Traber PG, Silberg DG (1996) Intestine-specific gene transcription. Annu Rev Physiol 58:275–297

    Article  PubMed  CAS  Google Scholar 

  • Trahair JF, Sangild PT (2004) Studying the development of the small intestine: philosophical and anatomical perspectives. In: Zabielski R, Gregory PC, Weström B (eds) Biology of the intestine in growing animals. Elsevier, Amsterdam, pp 1–54

    Google Scholar 

  • van Beers-Schreurs HM, Nabuurs MJ, Vellenga L, Kalsbeek-van der Valk HJ, Wensing T, Breukink HJ (1998) Weaning and the weanling diet influence the villous height and crypt depth in the small intestine of pigs and alter the concentrations of short-chain fatty acids in the large intestine and blood. J Nutr 128:947–953

    PubMed  Google Scholar 

  • van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, van der Horn K, Batlle E, Coudreuse D, Haramis AP, Tjon-Pon-Fong M, Moerer P, van den Born M, Soete G, Pals S, Eilers M, Medema R, Clevers H (2002) The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111:241–250

    Article  PubMed  Google Scholar 

  • van den Brink GR, Bleuming SA, Hardwick JC, Schepman BL, Offerhaus GJ, Keller JJ, Nielsen C, Gaffield W, van Deventer SJ, Roberts DJ, Peppelenbosch MP (2004) Indian Hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat Genet 36:277–282

    Article  PubMed  Google Scholar 

  • Weaver LT, Freiberg E, Israel EJ, Walker WA (1988) Epidermal growth factor in human amniotic fluid. Gastroenterology 95:1436

    PubMed  CAS  Google Scholar 

  • Williams EA, Rumsey RD, Powers HJ (1996) An investigation into the reversibility of the morphological and cytokinetic changes seen in the small intestine of riboflavin deficient rats. Gut 39:220–225

    Article  PubMed  CAS  Google Scholar 

  • Xu RJ, Zhang YQ (2003) Gastrointestinal regulatory peptides. In: Xu RJ, Granwell PD (eds) Neonatal pig gastrointestinal physiology and nutrition. Nottingham University Press, Nottingham, pp 61–93

    Google Scholar 

  • Xu RJ, Mao YL, Tso MY (1996) Stability of gastrin in the gastrointestinal lumen of suckling, weanling and adult pigs. Biol Neonate 70:60–68

    Article  PubMed  CAS  Google Scholar 

  • Xu RJ, Mellor DJ, Tungthanathanich P, Birtles MJ, Reynolds GW, Simpson HV (1992) Growth and morphological changes in the small and the large intestine in piglets during the first three days after birth. J Dev Physiol 18:161–172

    PubMed  CAS  Google Scholar 

  • Xu RJ, Wang F, Zhang SH (2000) Postnatal adaptation of the gastrointestinal tract in neonatal pigs: a possible role of milk-borne growth factors. Livestock Prod Sci 66:95–107

    Article  Google Scholar 

  • Xu RJ (1996) Development of the newborn GI tract and its relation to colostrum/milk intake: a review. Reprod Fertil Dev 8:35–48

    Article  PubMed  CAS  Google Scholar 

  • Yang C, Albin DM, Wang Z, Stoll B, Lackeyram D, Swanson KC, Yin Y, Tappenden KA, Mine Y, Yada RY, Burrin DG, Fan MZ (2011) Apical Na+-D-glucose cotransporter 1 (SGLT1) activity and protein abundance are expressed along the jejunal crypt-villus axis in the neonatal pig. Am J Physiol Gastrointest Liver Physiol 300:G60–G70

    Article  PubMed  CAS  Google Scholar 

  • Yang C (2011) Expression of porcine intestinal nutrient transporters along crypt-villus axis and during postnatal development. Doctoral dissertation, University of Guelph, Guelph, Ontario, Canada

    Google Scholar 

  • Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY (2001) Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294:2155–2158

    Article  PubMed  CAS  Google Scholar 

  • Yao K, Wang L, Ding BY, Fu DB, Liu YL, Zhu HL, Liu J, Li YT, Kang P, Yin YL, Wu GY, Hou YQ (2012a) Alpha-ketoglutarate inhibits glutamine degradation and enhances protein synthesis in intestinal porcine epithelial cells. Amino Acids 42(6):2491–2500

    Article  PubMed  CAS  Google Scholar 

  • Yeh KY, Yeh M, Montgomery RK, Grand RJ, Holt PR (1991) Cortisone and thyroxine modulate intestinal lactase and sucrase mRNA levels and activities in the suckling rat. Biochem Biophys Res Commun 180:174–180

    Article  PubMed  CAS  Google Scholar 

  • Zabielski R, Godlewski MM, Guilloteau P (2008) Control of development of gastrointestinal system in neonates. J Physiol Pharmacol 59(Suppl 1):35–54

    PubMed  Google Scholar 

  • Zabielski R (2007) Hormonal and neural regulation of intestinal function in pigs. Livest Sci 108:32–40

    Article  Google Scholar 

  • Zhang Y-G, Yin Y-L, Fang J, Wang Q (2012a) Pig production in subtropical agriculture. J Sci Food Agric 92:1016–1024

    Article  PubMed  CAS  Google Scholar 

  • Zweibaum A, Hauri HP, Sterchi E, Chantret I, Haffen K, Bamat J, Sordat B (1984) Immunohistological evidence, obtained with monoclonal antibodies, of small intestinal brush border hydrolases in human colon cancers and foetal colons. Int J Cancer 34:591–598

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yulong Yin .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Wien

About this chapter

Cite this chapter

Yang, H., Xiong, X., Yin, Y. (2013). Development and Renewal of Intestinal Villi in Pigs. In: Blachier, F., Wu, G., Yin, Y. (eds) Nutritional and Physiological Functions of Amino Acids in Pigs. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1328-8_3

Download citation

Publish with us

Policies and ethics