Skip to main content

The Comparative Anatomy of Islets

  • Chapter
  • First Online:
The Islets of Langerhans

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 654))

Abstract

In the past 20 years, numerous publications on a variety of mammalian and non-mammalian species have appeared in the literature to supplement the excellent comparative work performed in the 70s and 80s by the Falkmer, Epple, and Youson groups. What emerges is that islets are much more complex than once thought and show a lot of similarities in rodents and higher primates. The diversity of lifestyles, metabolic demands, and diets has most likely influenced the great diversity in both structure and cell-type content of islets in lower vertebrate species. In this chapter, I try to provide an overview of the evolution from endocrine cell types in invertebrates to the higher mammals and focus on what has been reported in the literature and some of our own experiences and also include a description of other hormones reported to be found in islets.

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 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
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

References

  1. Assouline B, Nguyen V, Mahe S, Bourrat F, Scharfmann R. Development of the pancreas in medaka, Mech Dev 2002;117:299–303.

    PubMed  CAS  Google Scholar 

  2. Kelly OG, Melton DA. Development of the pancreas in Xenopus laevis. Dev Dyn 2000;218(4):615–27.

    PubMed  CAS  Google Scholar 

  3. Kim SK, Hebrok M, Melton DA. Pancreas development in the chick embryo. Cold Spring Harb Symp Quant Biol 1997;62:377–83.

    PubMed  CAS  Google Scholar 

  4. Lammert E, Cleaver O, Melton D. Role of endothelial cells in early pancreas and liver development. Mech Dev 2003;120(1):59–64.

    PubMed  CAS  Google Scholar 

  5. Heller RS, Jenny M, Collombat P, Mansouri A, Tomasetto C, Madsen OD, Mellitzer G, Gradwohl G, Serup P. Genetic determinants of pancreatic epsilon-cell development. Dev Biol 20055;286(1):217–24.

    Google Scholar 

  6. Prado CL, Pugh-Bernard AE, Elghazi L, Sosa-Pineda B, Sussel L. Ghrelin cells replace insulin-producing beta cells in two mouse models of pancreas development. Proc Natl Acad Sci U S A 2004;101(9):2924–9.

    PubMed  CAS  Google Scholar 

  7. Wierup N, Svensson H, Mulder H, Sundler F. The ghrelin cell: a novel developmentally regulated islet cell in the human pancreas. Regul Pept 2002;107(1–3):63–9.

    PubMed  CAS  Google Scholar 

  8. Falkmer S and Ostberg Y. Comparative morphology of pancreatic islets in animals. In: The Diabetic Pancreas. Volk BW and Arquilla ER. Chap. 2. New York: Plenum Press; 1985

    Google Scholar 

  9. Smit AB, van Kesteren RE, Li KW, Van Minnen J, Spijker S, Van Heerikhuizen H, Geraerts WP. Towards understanding the role of insulin in the brain: lessons from insulin-related signaling systems in the invertebrate brain. Prog Neurobiol 1998;54(1): 35–54.

    PubMed  CAS  Google Scholar 

  10. Veenstra JA, Agricola HJ, Sellami A. Regulatory peptides in fruit fly midgut. Cell Tissue Res 2008; 334(3):499–516.

    PubMed  CAS  Google Scholar 

  11. Ikeya T, Galic M, Belawat P, Nairz K, Hafen E. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol 2002;12:1293–1300.

    PubMed  CAS  Google Scholar 

  12. Rulifson EJ, Kim SK, Nusse R. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 2002;296:1118–20.

    PubMed  CAS  Google Scholar 

  13. Veelaert D, Schoofs L, De Loof A. Peptidergic control of the corpus cardiacum-corpora allata complex of locusts. Int Rev Cytol 1998;182:249–302.

    PubMed  CAS  Google Scholar 

  14. Van der Horst D. Insect adipokinetic hormones: release and integration of flight energy metabolism. Comp Biochem Phys B 2003;136:217–26.

    Google Scholar 

  15. Kim SK, Rulifson EJ. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 2004;431:316–20.

    PubMed  CAS  Google Scholar 

  16. DeVelasco B, Shen J, Go S, Hartenstein V. Embryonic development of the Drosophila corpus cardiacum, a neuroendocrine gland with similarity to the vertebrate pituitary, is controlled by sine oculis and glass. Dev Biol 2004;274(2):280–94.

    CAS  Google Scholar 

  17. Ali-Rachedi A, Varndell IM, Adrian TE, Gapp DA, Van Noorden S, Bloom SR, Polak JM. Peptide YY (PYY) immunoreactivity is co-stored with glucagon-related immunoreactants in endocrine cells of the gut and pancreas. Histochemistry 1984;80(5):487–91.

    PubMed  CAS  Google Scholar 

  18. Galloway SM, Cutfield JF. Insulin-like material from the digestive tract of the tunicate Pyura pachydermatina (sea tulip). Gen Comp Endo 1988;69:106–13.

    CAS  Google Scholar 

  19. Epple A and Brinn JE. Pancreatic Islets. In: Vertebrate Endocrinology. Fundamentals and biomedical implications. Vol 1, chap 10. New York. Academic Press. 1986

    Google Scholar 

  20. Eberhard D, Tosh D, Slack JM. Origin of pancreatic endocrine cells from biliary duct epithelium. Cell Mol Life Sci 2008;65(21):3467–80.

    PubMed  CAS  Google Scholar 

  21. Yui R, Nagata Y, Fujita T. Immunocytochemical studies on the islet and the gut of the arctic lamprey, Lampetra japonica. Arch Histol Cytol 1988;51(1):109–19.

    PubMed  CAS  Google Scholar 

  22. Epple A, Cake MH, Potter IC, Tajbakhsh M. Impact of complete isletectomy on plasma glucose in the southern hemisphere lamprey Geotria australis. Gen Comp Endocrinol. 1992;86(2):284–8.

    PubMed  CAS  Google Scholar 

  23. Epple A and Brinn JE. Islet histophysiology. Evolutionary correlations. Gen Comp Endo 1975;27:320–49.

    CAS  Google Scholar 

  24. Kobayashi K, Syed Ali S. Cell types of the endocrine pancreas in the shark Scyliorhinus stellaris as revealed by correlative light and electron microscopy. Cell Tissue Res 1981;215(3):475–90.

    PubMed  CAS  Google Scholar 

  25. Brinn JE. Te pancreatic islets of bony fish. Am Zoologist 1973;13:652–6.

    Google Scholar 

  26. Briin JE and Epple A. new types of islet cells in a cyclostome, Petromyzon marinus. Cell Tissue Res 1976;171:317–29.

    Google Scholar 

  27. Hansen GN, Hansen BL, Jørgensen PN. Insulin-, glucagon- and somatostatin-like immunoreactivity in the endocrine pancreas of the lungfish, Neoceratodus forsteri. Cell Tissue Res. 1987;248(1):181–5.

    PubMed  CAS  Google Scholar 

  28. Youson, JH. Peripheral endocrine Glands. I. The gastoenteropancreatic endocrine system and the Thyroid Gland. Fish Physiology: Primitive Fishes 2007;Vol 26:381–425.

    Google Scholar 

  29. Field HA, Dong PD, Beis D, Stainier DY. Formation of the digestive system in zebrafish. II. Pancreas morphogenesis. Dev Biol 2003;261(1):197–208.

    PubMed  CAS  Google Scholar 

  30. Youson JH, Al-Mahrouki AA, Amemiya Y, Graham LC, Montpetit CJ, Irwin DM. The fish endocrine pancreas: review, new data, and future research directions in ontogeny and phylogeny. Gen Comp Endocrinol 2006;148(2):105–15.

    PubMed  CAS  Google Scholar 

  31. Youson JH, Al-Mahrouki AA. Ontogenetic and phylogenetic development of the endocrine pancreas (islet organ) in fish. Gen Comp Endocrinol 1999;116(3):303–35.

    PubMed  CAS  Google Scholar 

  32. Kaiya H, Small BC, Bilodeau AL, Shepherd BS, Kojima M, Hosoda H, Kangawa K. Purification, cDNA cloning, and characterization of ghrelin in channel catfish, Ictalurus punctatus. Gen Comp Endocrinol 2005;143(3):201–10.

    PubMed  CAS  Google Scholar 

  33. Ding WG, Kimura H, Fujimura M, Fujimiya M. Neuropeptide Y and peptide YY immunoreactivities in the pancreas of various vertebrates. Peptides 1997;18(10):1523–9.

    PubMed  CAS  Google Scholar 

  34. Epple A, Norris DA. Vertebrate Endocrinology. Philadelphia: Lea and Febiger; 1985.

    Google Scholar 

  35. Copeland PL and DeRoos R. Effect of mammalian insulin on plasma glucose in the mudpuppy, necturus maculosus. J Exp Zoology 1971;178:35–43.

    CAS  Google Scholar 

  36. Lee JH, Ku SK, Lee HS, Kitagawa H. An immunohistochemical study of endocrine cells in the pancreas of the Red-bellied frog (Bombina orientalis). Eur J Histochem. 2003;47(2):165–72.

    PubMed  Google Scholar 

  37. Kaiya H, Miyazato M, Kangawa K, Peter RE, Unniappan S. Ghrelin: a multifunctional hormone in non-mammalian vertebrates. Comp Biochem Physiol A Mol Integr Physiol. 2008;149(2):109–28.

    PubMed  Google Scholar 

  38. Reinecke M, Broger I, Brun R, Zapf J, Maake C. Immunohistochemical localization of insulin-like growth factor I and II in the endocrine pancreas of birds, reptiles, and amphibia. Gen Comp Endocrinol 1995;100(3):385–96.

    PubMed  CAS  Google Scholar 

  39. Ding WG, Kimura H, Fujimura M, Fujimiya M. Neuropeptide Y and peptide YY immunoreactivities in the pancreas of various vertebrates. Peptides 1997;18(10):1523–9.

    PubMed  CAS  Google Scholar 

  40. Norris DO. Vertebrate Endocrinology. Lea and Febiger; 1980.

    Google Scholar 

  41. Rhoten WB, Hall CE, Four hormones in the pancreas of the lizard, anolis carlinensis. Anat Rec 1981;199:89–97.

    PubMed  CAS  Google Scholar 

  42. Chandavar VR, Naik PR. Immunocytochemical detection of glucagon and insulin cells in endocrine pancreas and cyclic disparity of plasma glucose in the turtle Melanochelys trijuga. J Biosci 2008;33(2):239–47.

    PubMed  CAS  Google Scholar 

  43. Gapp DA, Kenny MP, Polak JM. The gastro-entero-pancreatic system of the turtle, Chrysemys picta. Peptides 6 Suppl 1985;3:347–52.

    Google Scholar 

  44. Kaiya H, Sakata I, Kojima M, Hosoda H, Sakai T, Kangawa K. Structural determination and histochemical localization of ghrelin in the red-eared slider turtle, Trachemys scripta elegans. Gen Comp Endocrinol. 2004;138(1):50–7.

    PubMed  CAS  Google Scholar 

  45. Masini MA. Immunocytochemical localization of peptides in the endocrine pancreas of the snakes Vipera aspis and Natrix maura. Acta Histochem. 1988;84(2):111–9.

    PubMed  CAS  Google Scholar 

  46. Falkmer S, Ostberg Y. The endocrine pancreas of birds Sitbon G, Mialhe P. J Physiol (Paris) 1980;76(1):5–24.

    Google Scholar 

  47. Simsek N, Ozüdoğru Z, Alabay B. Immunohistochemical studies on the splenic lobe of the pancreas in young Japanese quails (Coturnix c. japonica). Dtsch Tierarztl Wochenschr. 2008;115(5):189–93.

    PubMed  CAS  Google Scholar 

  48. Lucini C, Castaldo L, Lai O. An immunohistochemical study of the endocrine pancreas of ducks. Eur J Histochem. 1996;40(1):45–52.

    PubMed  CAS  Google Scholar 

  49. Edwin N, Leigh CM. The endocrine pancreas in the Australian wedge-tailed eagle (Aquila audax)—an immunocytochemical study. Eur J Histochem 1993;37(3):219–24.

    PubMed  CAS  Google Scholar 

  50. Mensah-Brown EP, Bailey TA, Pallot DJ, Garner A. Peptidergic hormones and neuropeptides, and aminergic neurotransmitters of the pancreatic islets of the Houbara bustard (Chlamydotis undulata). J Anat 2000;196 (Pt 2):233–41.

    PubMed  CAS  Google Scholar 

  51. Ding WG, Kimura H, Fujimura M, Fujimiya M. Neuropeptide Y and peptide YY immunoreactivities in the pancreas of various vertebrates. Peptides 1997;18(10):1523–9.

    PubMed  CAS  Google Scholar 

  52. López J, Cuesta N. Adrenomedullin as a pancreatic hormone. Microsc Res Tech 2002;57(2):61–75.

    PubMed  Google Scholar 

  53. Wieczorek G, Pospischil A, Perentes E. A comparative immunohistochemical study of pancreatic islets in laboratory animals (rats, dogs, minipigs, nonhuman primates). Exp Toxicol Pathol 1998;50(3):151–72.

    PubMed  CAS  Google Scholar 

  54. Gustavsen CR, Pillay N, Heller RS. An immunohistochemical study of the endocrine pancreas of the African ice rat, Otomys sloggetti robertsi. Acta Histochem 2008;110(4):294–301.

    PubMed  Google Scholar 

  55. Gustavsen CR, Chevret P, Krasnov B, Mowlavi G, Madsen OD, Heller RS. The morphology of islets of Langerhans is only mildly affected by the lack of Pdx-1 in the pancreas of adult Meriones jirds. Gen Comp Endocrinol 2008;159(2–3):241–9.

    PubMed  CAS  Google Scholar 

  56. Redecker P, Seipelt A, Jörns A, Bargsten G, Grube D. The microanatomy of canine islets of Langerhans: implications for intra-islet regulation. Anat Embryol (Berl) 1992;185(2):131–41.

    CAS  Google Scholar 

  57. Erasmus CP, Van Aswegen G. The endocrine pancreas of the Cape fur seal, Arctocephalus pusillus (Schreber, 1776): an immunocytochemical study. Onderstepoort J Vet Res 1997;64(3):239–42.

    PubMed  CAS  Google Scholar 

  58. Elvestad K, Henriques UV, Kroustrup JP. Insulin-producing islet cell tumor in an ectopic pancreas of a red fox (Vulpes vulpes). J Wildl Dis. 1984;20(1):70–2.

    PubMed  CAS  Google Scholar 

  59. Larsen MO, Rolin B. Use of the Göttingen minipig as a model of diabetes, with special focus on type 1 diabetes research. ILAR J 2004;45(3):303–13.

    PubMed  CAS  Google Scholar 

  60. Bellinger DA, Merricks EP, Nichols TC. Swine models of type 2 diabetes mellitus: insulin resistance, glucose tolerance, and cardiovascular complications. ILAR J. 2006;47(3):243–58.

    PubMed  CAS  Google Scholar 

  61. Adeghate E. Immunohistochemical identification of pancreatic hormones, neuropeptides and cytoskeletal proteins in pancreas of the camel (Camelus dromedarius). J Morphol 1997;231(2):185–93.

    PubMed  CAS  Google Scholar 

  62. Edwin N, Yamada J, Leigh CM. A light-microscopic immunocytochemical study of the endocrine pancreas in the Australian fat-tailed dunnart (Sminthopsis crassicaudata). Singapore Med J 1992;33(3):260–1.

    PubMed  CAS  Google Scholar 

  63. Leigh CM, Edwin N. A light-microscopic immunocytochemical study of the endocrine pancreas in the Australian brush tailed possum (Trichosurus vulpecula). Eur J Histochem 1992;36(2):237–41.

    PubMed  CAS  Google Scholar 

  64. Reddy S, Bibby NJ, Fisher SL, Elliott RB Immunolocalization of insulin, glucagon, pancreatic polypeptide, and somatostatin in the pancreatic islets of the possum, Trichosurus vulpecula. Gen Comp Endocrinol 1986;64(1):157–62.

    PubMed  CAS  Google Scholar 

  65. Krause WJ, Cutts JH 3rd, Cutts JH, Yamada J. Immunohistochemical study of the developing endocrine pancreas of the opossum (Didelphis virginiana). Acta Anat (Basel) 1989;135(1):84–96.

    CAS  Google Scholar 

  66. Menzies BR, Shaw G, Fletcher TP, Renfree MB. Early onset of ghrelin production in a marsupial. Mol Cell Endocrinol. 2009;299(2):266–73.

    PubMed  CAS  Google Scholar 

  67. Michelmore AJ, Keegan DJ, Kramer B. Rousettus aegyptiacus. Immunocytochemical identification of endocrine cells in the pancreas of the fruit bat, Gen Comp Endocrinol 1998;110(3):319–25.

    PubMed  CAS  Google Scholar 

  68. Bamroongwong S, Chunhabundit P, Rattanchaikunsopon P, Somana R. Pancreatic microcirculation in the common tree shrew (Tupaia glis) as revealed by scanning electron microscopy of vascular corrosion casts. Acta Anat (Basel)1992;143(3):188–94.

    CAS  Google Scholar 

  69. Sujatha SR, Pulimood A, Gunasekaran S. Comparative immunocytochemistry of isolated rat & monkey pancreatic islet cell types. Indian J Med Res 2004;119(1):38–44.

    PubMed  Google Scholar 

  70. Madsen OD, Serup P, Jensen J, Petersen HV, Heller RS. A historical and phylogenetic perspective of the understanding of islet cell development. In: Molecular basis of endocrine pancreas development and function. Hussain MA, Miller CP and Habener, JF, editors. Boston: Kluwer Academic Publishers; 2000.

    Google Scholar 

  71. Ahnfelt-Rønne J, Jørgensen MC, Hald J, Madsen OD, Serup P, Hecksher-Sørensen J. An improved method for three-dimensional reconstruction of protein expression patterns in intact mouse and chicken embryos and organs. J Histochem Cytochem 2007;55(9):925–30.

    PubMed  Google Scholar 

  72. Jørgensen MC, Ahnfelt-Rønne J, Hald J, Madsen OD, Serup P, Hecksher-Sørensen J. An illustrated review of early pancreas development in the mouse. Endocr Rev 2007;28(6):685–705.

    PubMed  Google Scholar 

  73. Alanentalo T, Asayesh A, Morrison H, Lorén CE, Holmberg D, Sharpe J, Ahlgren U. Tomographic molecular imaging and 3D quantification within adult mouse organs. Nat Methods 2007;4(1):31–3.

    PubMed  CAS  Google Scholar 

  74. Holmberg D, Ahlgren U. Imaging the pancreas: from ex vivo to non-invasive technology. Diabetologia. 2008;51(12):2148–54.

    PubMed  CAS  Google Scholar 

  75. Wierup N, Kuhar M, Nilsson BO, Mulder H, Ekblad E, Sundler F. Cocaine- and amphetamine-regulated transcript (CART) is expressed in several islet cell types during rat development. J Histochem Cytochem 2004;52(2):169–77.

    PubMed  CAS  Google Scholar 

  76. Arciszewski MB, Całka J, Majewski M. Cocaine- and amphetamine-regulated transcript (CART) is expressed in the ovine pancreas. Ann Anat 2008;190(3):292–9.

    PubMed  Google Scholar 

  77. Jönsson AC. Endocrine cells with gastrin/cholecystokinin-like immunoreactivity in the pancreas of the spiny dogfish, Squalus acanthias. Regul Pept 1995;59(1):67–78.

    PubMed  Google Scholar 

  78. Shimizu K, Kato Y, Shiratori K, Ding Y, Song Y, Furlanetto R, Chang TM, Watanabe S, Hayashi N, Kobayashi M, Chey WY. Evidence for the existence of CCK-producing cells in rat pancreatic islets. Endocrinology 1998;139(1):389–96.

    PubMed  CAS  Google Scholar 

  79. Fujimura M, Greeley GH Jr, Hancock MB, Alwmark A, Santos A, Cooper CW, Reumont KJ, Ishizuka J, Thompson JC. Colocalization of calcitonin gene-related peptide and somatostatin in pancreatic islet cells and inhibition of insulin secretion by calcitonin gene-related peptide in the rat. Pancreas 1988;3(1):49–52.

    PubMed  CAS  Google Scholar 

  80. Böttcher G, Sjöberg J, Ekman R, Håkanson R, Sundler F. Peptide YY in the mammalian pancreas: immunocytochemical localization and immunochemical characterization. Regul Pept 1993;43(3):115–30.

    PubMed  Google Scholar 

  81. Jackerott M, Oster A, Larsson LI. PYY in developing murine islet cells: comparisons to development of islet hormones, NPY, and BrdU incorporation. J Histochem Cytochem 1996;44(8):809–17.

    PubMed  CAS  Google Scholar 

  82. Navarro MH, Lozano MT, Agulleiro B. Ontogeny of the endocrine pancreatic cells of the gilthead sea bream, Sparus aurata (Teleost). Gen Comp Endocrinol 2006;148(2):213–26.

    PubMed  CAS  Google Scholar 

  83. Nascimento AA, Sales A, Cardoso TR, Pinheiro NL, Mendes RM. Immunocytochemical study of the distribuition of endocrine cells in the pancreas of the Brazilian sparrow species Zonotrichia Capensis Subtorquata (Swaison, 1837). Braz J Biol 2007;67(4):735–40.

    PubMed  CAS  Google Scholar 

  84. Gustavsen CR, Kvicerova J, Dickinson H, Heller RS. Acomys, the closest relatives to Gerbils do express Pdx-1 and have similar islet morphology. Islets 2009:1(3).

    Google Scholar 

  85. Fujita T, Yui R, Iwanaga T, Nishiitsutsuji-Uwo J, Endo Y, Yanaihara N. Evolutionary aspects of “brain-gut peptides”: an immunohistochemical study. Peptides 1981;2 Suppl 2:123–31.

    PubMed  CAS  Google Scholar 

  86. Kawano H, Daikoku S, Saito S. Location of thyrotropin-releasing hormone-like immunoreactivity in rat pancreas. Endocrinology 1983;112(3):951–5.

    PubMed  CAS  Google Scholar 

  87. Tsuruo Y, Hökfelt T, Visser TJ, Kimmel JR, Brown JC, Verhofstadt A, Walsh J. TRH-like immunoreactivity in endocrine cells and neurons in the gastro-intestinal tract of the rat and guinea pig. Cell Tissue Res 1988;253(2):347–56.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I would like to thank Nils Wierup, Carsten Godfredsen, and Yana Kvicerova for providing some of the tissue samples used in Fig. 2.4. I would also like to thank my graduate student Carsten Gustavsen for his excellent work in this area of comparative morphological analysis of different species and finally Jan Nygård Jensen, Ole Madsen, and Carsten Gustavsen for helpful comments on the chapter.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Scott Heller .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Heller, R.S. (2010). The Comparative Anatomy of Islets. In: Islam, M. (eds) The Islets of Langerhans. Advances in Experimental Medicine and Biology, vol 654. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3271-3_2

Download citation

Publish with us

Policies and ethics