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Zoomorphology

, Volume 137, Issue 3, pp 419–432 | Cite as

Histological organization of intestinal villi in the crocodilian caiman yacare (Daudin, 1802) during dietary lipid absorption

  • Ricardo Moraes BorgesEmail author
  • Leandro Nogueira Pressinotti
  • Francisco Alberto Marcus
  • Renata Stecca Iunes
  • Victor Manuel Aleixo
  • Tânia Cristina Lima Portela
  • João Carlos Shimada Borges
  • Alessandro Spíndola Bérgamo
  • Ângela Paula Alves de Lima
  • José Roberto Machado Cunha da Silva
Original paper
  • 144 Downloads

Abstract

Intestinal villi of Caiman yacare form longitudinal folds instead of the finger-like projections of most birds and mammals. Moreover, they lack Crypts of Lieberkühn and the lamina epithelialis organization is dynamic, changing from pseudostratified to simple columnar epithelium after feeding. Because of these differences, we sought to verify whether intestinal villi of the crocodilian Caiman yacare are functionally compartmentalized along their length similarly to the finger-like villi that harbors Crypt of Lieberkühn. For this, Caiman yacare were force-fed soybean oil, the intestinal mucosa was harvested and analyzed under light microscopy after lipid staining or immunohistochemistry for the proliferative marker PCNA. Functional compartmentalization was assessed by evaluating differences in lipid absorption along intestinal villi base-to-tip axis, by localizing the proliferative enterocytes and by verifying whether such cells were capable of absorbing lipids. Histological morphometric analyses of the extent of enterocyte hypertrophy caused by lipid inclusions and the contribution of such inclusions to histological remodeling from pseudostratified to simple columnar epithelium were also evaluated. Although lacking Crypts of Lieberkühn, enterocytes present at villi base were PCNA positive and devoid of the great amount of lipid inclusions observed in the other intestinal villi domains, in a similar pattern to finger-like villi. Enterocytes doubled their volume because of lipid inclusions, and in spite of such enterocyte hypertrophy, lamina epithelialis continued to be pseudostratified within lateral sides, whereas villi tip were organized in a simple columnar epithelium.

Keywords

Intestinal villi Crypt of Lieberkühn Proliferative intestinal stem cells Lipid absorption Non-avian sauropsids Crocodilian 

Notes

Acknowledgements

The authors would like to thank: COOCRIJAPAN (Cooperativa dos Criadores de Jacaré-do-Pantanal) for donating the animals used in the experiments and for sharing the facilities; Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)/São Paulo Research Foundation for supporting this work.

Funding

This work was supported by Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT) contract Grant Number 715823/2008 and by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)/São Paulo Research Foundation contract Grant Number 2010/04527-5. RMB has received a scholarship from FAPESP, contract Grant Number 09/52884-4.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Animal handling and experimentation were approved by the committee on animal welfare and ethical experimentation from Institute of Biomedical Sciences, University of Sao Paulo (Protocol Number 131, page 110, book 02; issued September 20th, 2011) and by Brazilian environmental agency (ICMBIO/MMA/SISBIO: authorization number 30509-2; issued August 30th, 2011).

References

  1. Abumrad NA, Davidson NO (2012) Role of the gut in lipid homeostasis. Physiol Rev 92:1061–1085.  https://doi.org/10.1152/physrev.00019.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aleixo VM, Cotta T, Logato PVR, Oliveira AIG, Fialho ET (2002) Efeitos da adição de diferentes teores de farelo de soja na dieta sobre o desenvolvimento de filhotes de jacaré-do-pantanal [Caiman yacare(Daudin, 1802)]. Cienc Agrotec 26:411–417Google Scholar
  3. Aleixo VM, Pressinotti LN, Campos DVS, Menezes-Aleixo RC, Ferraz RHS (2011) Histologia, histoquímica e histometria do intestino de jacaré-do-pantanal criado em cativeiro. Pesq Vet Bras 31:1120–1128.  https://doi.org/10.1590/S0100-736X2011001200014 CrossRefGoogle Scholar
  4. Alpers DH, Bass NM, Engle MJ, DeSchryver-Kecskemei (2000) Intestinal fatty acid binding protein may favor differential apical fatty acid binding in the intestine. Biochim Biophys Acta 1483:352–362.  https://doi.org/10.1016/S1388-1981(99)00200-0 CrossRefPubMedGoogle Scholar
  5. Andrew AL, Card DC, Ruggiero RP, Schield DR, Adams RH, Pollock DD, Secor SM, Castoe TA (2015) Rapid changes in gene expression direct rapid shifts in intestinal form and function in the Burmese python after feeding. Physiol Genom 47:147–157.  https://doi.org/10.1152/physiolgenomics.00131.2014 CrossRefGoogle Scholar
  6. Barker N (2014) Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat Rev Mol Cell Biol 15:19–33.  https://doi.org/10.1038/nrm3721 CrossRefPubMedGoogle Scholar
  7. Bateman PA, Jackon KG, Maitin V, Yaqoob P, Willians CM (2007) Differences in cell morphology, lipid and apo B secretory capacity in caco-2 cells following long term treatment with saturated and monounsaturated fatty acids. Biochim Biophys Acta 1771:475–485.  https://doi.org/10.1016/j.bbalip.2007.02.001 CrossRefPubMedGoogle Scholar
  8. Borges RM, Pressinotti LN, Aleixo VM, Borges JCS, Bérgamo AS, Iunes RS, Silva JRMC. (2016) Dietary lipid absorption and lipoprotein secretion by the intestine of the crocodilianCaiman yacare(Daudin, 1802). Zoomorphology.  https://doi.org/10.1007/s00435-015-0300-9 CrossRefGoogle Scholar
  9. Campos Z, Coutinho M, Magnusson WE (2006) Caiman crocodilus yacare (Pantanal caiman). Aestivation Herpetol Rev 37:343–344Google Scholar
  10. Danielsen EM, Hansen GH, Rasmussen K, Niels-Christiansen LL (2013) Permeabilization of enterocytes induced by absorption of dietary fat. Mol Membr Biol 30:261–272.  https://doi.org/10.3109/09687688.2013.780642 CrossRefPubMedGoogle Scholar
  11. Ferri S, Junqueira LC, Medeiros LF, Medeiros LO (1976) Gross, microscopic and ultrastructural study of the intestinal tube of Xenodon merremiiWagler, 1824 (Ophidia). J Anat 121:291–301PubMedPubMedCentralGoogle Scholar
  12. Gajda AM, Storch J (2015) Enterocyte fatty acid binding proteins (FABPs): different functions of liver- and intestinal FABPs in the intestine. Prostaglandins Leukot Essent Fatty Acids 93:9–16.  https://doi.org/10.1016/j.plefa.2014.10.001 CrossRefPubMedGoogle Scholar
  13. Guilmeau S, Niot I, Laigneau JP, Devaud H, Petit V, Brousse N, Bouvier R, Ferkdaji L, Besmond C, Aggerbeck LP, Bado A, Samson-Bouma ME (2007) Decreased expression of intestinal I- and F-FABP levels in rare human genetic lipid malabsorption syndromes. Histocehm Cell Biol 128:115–123.  https://doi.org/10.1007/s00418-007-0302-x CrossRefGoogle Scholar
  14. Hayashi H, Maruyama S, Fukuoka M, Kozakai T, Nakajima K, Onaga T, Kato S (2013) Fatty acid-binding protein expression in the gastrointestinal tract of calves and cows. Anim Sci J 84:35–44.  https://doi.org/10.1111/j.1740-0929.2012.01038.x CrossRefPubMedGoogle Scholar
  15. Helmstetter C, Reix N, T´Flachebba M, Pope RK, Secor SM, Le Maho Y, Lignot JH (2009a) Functional changes with feeding in the gastro-intestinal epithelia of the Burmese pyton (Python molurus). Zool Sci 26:632–638.  https://doi.org/10.2108/zsj.26.632 CrossRefPubMedGoogle Scholar
  16. Helmstetter C, Pope RK, T´Flachebba M, Secor SM, Lignot JH (2009b) The effects of feeding on cell morphology and proliferation of the gastrointestinal tract of juvenile Burmese pythons (Python molurus). Can J Zool 87:1255–1267.  https://doi.org/10.1139/Z09-110 CrossRefGoogle Scholar
  17. Jackson K, Perry G (2000) Changes in intestinal morphology following feeding in the brown treesnake, Boiga irregularis. J Herpetol 34:459–462.  https://doi.org/10.2307/1565371 CrossRefGoogle Scholar
  18. Jacobson ER (2007) Overview of reptile biology, anatomy and histology. In: Jaratoncobson ER (ed) Infectious diseases and pathology of Reptiles, color atlas and text. CRC Press, Boca Raton, pp 1–30.  https://doi.org/10.1201/9781420004038.ch1
  19. Jin SM, Maruch SMG, Rodrigues MAM, Pacheco P (1991) Histologia geral dos intestinos do Caiman crocodilus yacare(DAUDIN, 1802) (Crocodilia:Reptilia). Rev Bras Zool 7:111–120.  https://doi.org/10.1590/S0101-81751990000200011 CrossRefGoogle Scholar
  20. Johnson TS, Dornfeld EJ, Conte FP (1967) Cellular renewal of intestinal epithelium in the western fence lizard, Sceloporus occidentalis. Can J Zool 45:63–71.  https://doi.org/10.1139/z67-008 CrossRefGoogle Scholar
  21. Kiesslich R, Goetz M, Angus EM, Hu Q, Guan Y, Potten C, Allen T, Neurath MF, Shroeyer NF, Montrose MH, Watson AJM (2007) Identification of epithelial gaps in human small and large intestine by confocal endomicroscopy. Gastroenterology 133:1769–1778.  https://doi.org/10.1053/j.gastro.2007.09.011 CrossRefPubMedGoogle Scholar
  22. Kubben FJ, Peeters-Haesevoets A, Engels LG, Baeten CG, Schutte B, Arends JW, Stockbrüggers RW, Blijham GH (1994) Proliferating cell nuclear antigen (PCNA): a new marker to study human colonic cell proliferation. Gut 35:530–535CrossRefPubMedPubMedCentralGoogle Scholar
  23. Levy E, Ménard D, Delvin E, Montoudis A, Beaulieu JF, Mailhot G, Dubé N, Sinnett D, Seidman E, Bendayan M (2009) Localization, function and regulation of the two intestinal fatty acid-binding protein types. Histochem Cell Biol 132:351–367.  https://doi.org/10.1007/s00418-009-0608-y CrossRefPubMedGoogle Scholar
  24. Lignot JH, Helmstetter C, Secor SM (2005) Postprandial morphological response of the intestinal epithelium of the Burmese python(Python molurus). Comp Biochem Physiol A Mol Integr Physiol 141:280–291.  https://doi.org/10.1016/j.cbpb.2005.05.005 CrossRefPubMedGoogle Scholar
  25. Magalhães MS, Freitas ML, Silva NB, Moura CEB (2010) Morfologia do tubo digestório da tartaruga verde (Chelonia mydas). Pesq Vet Bras 30:676–684.  https://doi.org/10.1590/S0100-736X2010000800012 CrossRefGoogle Scholar
  26. McCue MD, Guzman M, Passement CA (2015) Digesting pythons quickly oxidize the proteins in their meals and save the lipids for later. J Exp Biol 218:2089–2096CrossRefPubMedGoogle Scholar
  27. McCue MD, Passement CA, Meyerholz DK (2017) Maintenance of distal intestinal structure in the face of prolonged fasting: a comparative examination of species from five vertebrate classes. Anat Rec 300:2208–2219CrossRefGoogle Scholar
  28. McDonald JH (2014) Handbook of biological statistics, 3rd (ed). Sparky House Publishing, BaltimoreGoogle Scholar
  29. Ott BD, Secor SM (2007) Adaptive regulation of digestive performance in the genus Python. J Exp Biol 210:340–356.  https://doi.org/10.1242/jeb.02626 CrossRefPubMedGoogle Scholar
  30. Parsons TS, Cameron JE (1977) Internal relief of the digestive tract. In: Gans C, Parsons TS (eds) Biology of the reptilian. Academic Press, New York, pp 159–224Google Scholar
  31. Pressinotti LN, Borges RM, Alves de Lima AP, Aleixo VM, Iunes RS, Borges JC, Bogliati B, Cunha da Silva JR (2013) Low temperature reduces skin healing in the jacaré do pantanal (Caiman yacare, Daudin 1802). Biol Open 2:1171–1178.  https://doi.org/10.1242/bio.20135876 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Rodrigues-Sartori SS, Nogueira KOPC., Rocha AS, Neves CA (2014) Functional morphology of the gut of the tropical house gecko Hemidactylus mabouia(Squamata: Gekkonidae). Anim Biol 64:217–237.  https://doi.org/10.1163/15707563-00002443 CrossRefGoogle Scholar
  33. Sailaja BS, He XC, Li L (2016) Regulatory niche in intestinal stem cells. J Physiol.  https://doi.org/10.1113/JP271931 (Accepted Author manuscript)PubMedPubMedCentralCrossRefGoogle Scholar
  34. Santos SA, Nogueira MS, Pinheiro MS, Campos Z, Magnusson WE, Mourão GM (1996) Diets of Caiman crocodilus yacare from different habitats in the Brazilian Pantanal. Herpetological J 6:111–1117Google Scholar
  35. Secor SM (2005) Evolutionary and cellular mechanisms regulating intestinal performance of amphibians and reptiles. Integr Comp Biol 45:282–294.  https://doi.org/10.1093/icb/45.2.282 CrossRefPubMedGoogle Scholar
  36. Secor SM, Diamond J (1999) Maintenance of digestive performance in the turtle Chelydra serpentina, Sternotherus odoratus, and Trachemys scripta. Copeia 1:75–84.  https://doi.org/10.2307/1447387 CrossRefGoogle Scholar
  37. Secor SM, Diamond JM (2000) Evolution of regulatory responses to feeding in snakes. Physiol Biochem Zool 73:123–141.  https://doi.org/10.1086/316734
  38. Secor SM, Lane JS, Whang EE, Ashley SW, Diamond J (2002) Luminal nutrient signals for intestinal adaptation in pythons. Am J Physiol Gastrointest Liver Physiol 283:G1298–G1309.  https://doi.org/10.1152/ajpgi.00194.2002 CrossRefPubMedGoogle Scholar
  39. Starck JM, Beese K (2001) Structural flexibility of the intestine of Burmese python in response to feeding. J Exp Biol 204:325–335PubMedGoogle Scholar
  40. Starck JM, Beese K (2002) Structural flexibility of the small intestine and liver of garter snakes in response to feeding and fasting. J Exp Biol 205:1377–1388PubMedGoogle Scholar
  41. Starck JM, Wimmer C (2005) Patterns of blood flow during the postprandial response in ball pythons, Python regius. J Exp Biol 208:881–889.  https://doi.org/10.1242/jeb.01478 CrossRefPubMedGoogle Scholar
  42. Starck JM, Cruz-Neto AP, Abe AS (2007) Physiological and morphological responses to feeding in broad-nosed caiman (Caiman latirostris). J Exp Biol 210:2035–2045.  https://doi.org/10.1242/jeb.000976 CrossRefGoogle Scholar
  43. Tracy CR, McWhorter TJ, Gienger CM, Starck JM, Medley P, Manolis SC, Webb GJ, Christian KA (2015) Alligators and crocodiles have high paracellular absorption of nutrients, but differ in digestive morphology and physiology. Integr Comp Biol 55:986–1004.  https://doi.org/10.1093/icb/icv060 CrossRefPubMedGoogle Scholar
  44. Watson AJM, Duckworth CA, Guan Y, Montrose MH (2009) Mechanisms of epithelial cell shedding in the mammalian intestine and maintenance of barrier function. Ann N Y Acad Sci 1165:135–142.  https://doi.org/10.1111/j.1749-6632.2009.04027.x CrossRefPubMedGoogle Scholar
  45. Williams JM, Duckworth CA, Burkitt MD, Watson AJ, Campbell BJ, Pritchard DM (2015) Epithelial cell shedding and barrier function: a matter of life and death at the small intestinal villus tip. Vet Pathol 52:445–455.  https://doi.org/10.1177/0300985814559404 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Wurth MA, Musacchia XJ (1964) Renewal of intestinal epithelium in the freshwater turtle Chrysemys picta. Anat Rec 148:427–439.  https://doi.org/10.1002/ar.1091480302 CrossRefPubMedGoogle Scholar
  47. Yu T, Chen QK, Gong Y, Xia ZS, Royal CR, Huang KH (2010) Higher expression patterns of the intestinal stem cell markers Musashi-1 and hairy and enhancer of split 1 and their correspondence with proliferation patterns in the mouse jejunum. Med Sci Monit 16:BR68–74PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ricardo Moraes Borges
    • 1
    Email author
  • Leandro Nogueira Pressinotti
    • 1
    • 2
  • Francisco Alberto Marcus
    • 3
  • Renata Stecca Iunes
    • 1
  • Victor Manuel Aleixo
    • 4
  • Tânia Cristina Lima Portela
    • 1
  • João Carlos Shimada Borges
    • 1
    • 5
  • Alessandro Spíndola Bérgamo
    • 2
    • 6
  • Ângela Paula Alves de Lima
    • 2
  • José Roberto Machado Cunha da Silva
    • 1
    • 7
  1. 1.Departamento de Biologia Celular e do Desenvolvimento, Instituto de Ciências BiomédicasUniversidade de São Paulo (USP), Cidade UniversitáriaSão PauloBrazil
  2. 2.Departamento de Ciências BiológicasUniversidade do Estado de Mato Grosso (UNEMAT)CáceresBrazil
  3. 3.Departamento de Física Aplicada, Instituto de FísicaUniversidade de São Paulo (USP)São PauloBrazil
  4. 4.Instituto Federal de Educação Ciência e Tecnologia de Mato Grosso (IFMT)-Campus CáceresCáceresBrazil
  5. 5.Faculdade de Medicina VeterináriaCentro Universitário das Faculdades Metropolitanas Unidas (UniFMU)São PauloBrazil
  6. 6.Cooperativa de Criadores de Jacaré do Pantanal (COOCRIJAPAN)CáceresBrazil
  7. 7.Centro de Biologia Marinha (CeBiMar)Universidade de São Paulo (USP)São SebastiãoBrazil

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