Skip to main content

The Comparative Anatomy of Islets

  • Reference work entry
  • First Online:
Islets of Langerhans

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 1970s and 1980s 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 699.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 549.99
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

  • Adeghate E (1997) Immunohistochemical identification of pancreatic hormones, neuropeptides and cytoskeletal proteins in pancreas of the camel (Camelus dromedarius). J Morphol 231(2):185–193

    Article  PubMed  CAS  Google Scholar 

  • Ahnfelt-Rønne J, Jørgensen MC, Hald J, Madsen OD, Serup P, Hecksher-Sørensen J (2007) An improved method for three-dimensional reconstruction of protein expression patterns in intact mouse and chicken embryos and organs. J Histochem Cytochem 55(9):925–930

    Article  PubMed  Google Scholar 

  • Alanentalo T, Asayesh A, Morrison H, Lorén CE, Holmberg D, Sharpe J, Ahlgren U (2007) Tomographic molecular imaging and 3D quantification within adult mouse organs. Nat Methods 4(1):31–33

    Article  PubMed  CAS  Google Scholar 

  • Ali-Rachedi A, Varndell IM, Adrian TE, Gapp DA, Van Noorden S, Bloom SR, Polak JM (1984) Peptide YY (PYY) immunoreactivity is co-stored with glucagon-related immunoreactants in endocrine cells of the gut and pancreas. Histochemistry 80(5):487–491

    Article  PubMed  CAS  Google Scholar 

  • Arciszewski MB, Całka J, Majewski M (2008) Cocaine-and amphetamine-regulated transcript (CART) is expressed in the ovine pancreas. Ann Anat 190(3):292–299

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bamroongwong S, Chunhabundit P, Rattanchaikunsopon P, Somana R (1992) Pancreatic microcirculation in the common tree shrew (Tupaia glis) as revealed by scanning electron microscopy of vascular corrosion casts. Acta Anat (Basel) 143(3):188–194

    Article  CAS  Google Scholar 

  • Bellinger DA, Merricks EP, Nichols TC (2006) Swine models of type 2 diabetes mellitus: insulin resistance, glucose tolerance, and cardiovascular complications. ILAR J 47(3):243–258

    Article  PubMed  CAS  Google Scholar 

  • Böttcher G, Sjöberg J, Ekman R, Håkanson R, Sundler F (1993) Peptide YY in the mammalian pancreas: immunocytochemical localization and immunochemical characterization. Regul Pept 43(3):115–130

    Article  PubMed  Google Scholar 

  • Briin JE, Epple A (1976) New types of islet cells in a cyclostome, Petromyzon marinus. Cell Tissue Res 171:317–329

    Google Scholar 

  • Brinn JE (1973) Te pancreatic islets of bony fish. Am Zool 13:652–656

    Google Scholar 

  • Chandavar VR, Naik PR (2008) Immunocytochemical detection of glucagon and insulin cells in endocrine pancreas and cyclic disparity of plasma glucose in the turtle Melanochelys trijuga. J Biosci 33(2):239–247

    Article  PubMed  CAS  Google Scholar 

  • Copeland PL, DeRoos R (1971) Effect of mammalian insulin on plasma glucose in the mud puppy, necturus maculosus. J Exp Zool 178:35–43

    Article  PubMed  CAS  Google Scholar 

  • DeVelasco B, Shen J, Go S, Hartenstein V (2004) 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 274(2):280–294

    Article  CAS  Google Scholar 

  • Ding WG, Kimura H, Fujimura M, Fujimiya M (1997) Neuropeptide Y and peptide YY immunoreactivities in the pancreas of various vertebrates. Peptides 18(10):1523–1529

    Article  PubMed  CAS  Google Scholar 

  • Eberhard D, Tosh D, Slack JM (2008) Origin of pancreatic endocrine cells from biliary duct epithelium. Cell Mol Life Sci 65(21):3467–3480

    Article  PubMed  CAS  Google Scholar 

  • Edwin N, Leigh CM (1993) The endocrine pancreas in the Australian wedge-tailed eagle (Aquila audax) – an immunocytochemical study. Eur J Histochem 37(3):219–224

    PubMed  CAS  Google Scholar 

  • Edwin N, Yamada J, Leigh CM (1992) A light-microscopic immunocytochemical study of the endocrine pancreas in the Australian fat-tailed dunnart (Sminthopsis crassicaudata). Singap Med J 33(3):260–261

    CAS  Google Scholar 

  • Elvestad K, Henriques UV, Kroustrup JP (1984) Insulin-producing islet cell tumor in an ectopic pancreas of a red fox (Vulpes vulpes). J Wildl Dis 20(1):70–72

    Article  PubMed  CAS  Google Scholar 

  • Epple A, Brinn JE (1975) Islet histophysiology. Evolutionary correlations. Gen Comp Endocrinol 27:320–349

    Article  PubMed  CAS  Google Scholar 

  • Epple A, Brinn JE (1986) Chap 10: Pancreatic islets. In: Vertebrate endocrinology. Fundamentals and biomedical implications, vol 1. Academic, New York

    Google Scholar 

  • Epple A, Norris DA (1985) Vertebrate endocrinology. Lea and Febiger, Philadelphia

    Google Scholar 

  • Epple A, Cake MH, Potter IC, Tajbakhsh M (1992) Impact of complete isletectomy on plasma glucose in the southern hemisphere lamprey Geotria australis. Gen Comp Endocrinol 86(2):284–288

    Article  PubMed  CAS  Google Scholar 

  • Erasmus CP, Van Aswegen G (1997) The endocrine pancreas of the Cape fur seal, Arctocephaluspusillus (Schreber, 1776): an immunocytochemical study. Onderstepoort J Vet Res 64(3):239–242

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Falkmer S, Ostberg Y (1985) Chap 2: Comparative morphology of pancreatic islets in animals. In: Volk BW, Arquilla ER (eds) The diabetic pancreas. Plenum Press, New York

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fujimura M, Greeley GH Jr, Hancock MB, Alwmark A, Santos A, Cooper CW, Reumont KJ, Ishizuka J, Thompson JC (1988) 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 3(1):49–52

    Article  PubMed  CAS  Google Scholar 

  • Fujita T, Yui R, Iwanaga T, Nishiitsutsuji-Uwo J, Endo Y, Yanaihara N (1981) Evolutionary aspects of “brain-gut peptides”: an immunohistochemical study. Peptides 2(Suppl 2):123–131

    Article  PubMed  CAS  Google Scholar 

  • Galloway SM, Cutfield JF (1988) Insulin-like material from the digestive tract of the tunicate Pyura pachydermatina (sea tulip). Gen Comp Endocrinol 69:106–113

    Article  PubMed  CAS  Google Scholar 

  • Gapp DA, Kenny MP, Polak JM (1985) The gastro-entero-pancreatic system of the turtle, Chrysemyspicta. Peptides 3(6 Suppl):347–352

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gustavsen CR, Chevret P, Krasnov B, Mowlavi G, Madsen OD, Heller RS (2008b) 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 159(2–3):241–249

    Article  PubMed  CAS  Google Scholar 

  • Gustavsen CR, Kvicerova J, Dickinson H, Heller RS (2009) Acomys, the closest relatives to Gerbils do express Pdx-1 and have similar islet morphology. Islets 1(3):191

    Article  PubMed  Google Scholar 

  • Hansen GN, Hansen BL, Jørgensen PN (1987) Insulin-, glucagon- and somatostatin-like immunoreactivity in the endocrine pancreas of the lungfish, Neoceratodus forsteri. Cell Tissue Res 248(1):181–185

    Article  PubMed  CAS  Google Scholar 

  • Heller RS, Jenny M, Collombat P, Mansouri A, Tomasetto C, Madsen OD, Mellitzer G, Gradwohl G, Serup P (2005) Genetic determinants of pancreatic ε-cell development. Dev Biol 286(1):217–224

    Article  PubMed  CAS  Google Scholar 

  • Holmberg D, Ahlgren U (2008) Imaging the pancreas: from ex vivo to non-invasive technology. Diabetologia 51(12):2148–2154

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jackerott M, Oster A, Larsson LI (1996) PYY in developing murine islet cells: comparisons to development of islet hormones, NPY, and BrdU incorporation. J Histochem Cytochem 44(8):809–817

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kaiya H, Sakata I, Kojima M, Hosoda H, Sakai T, Kangawa K (2004) Structural determination and histochemical localization of ghrelin in the red-eared slider turtle, Trachemys scripta elegans. Gen Comp Endocrinol 138(1):50–57

    Article  PubMed  CAS  Google Scholar 

  • Kaiya H, Small BC, Bilodeau AL, Shepherd BS, Kojima M, Hosoda H, Kangawa K (2005) Purification, cDNA cloning, and characterization of ghrelin in channel catfish, Ictaluruspunctatus. Gen Comp Endocrinol 143(3):201–210

    Article  PubMed  CAS  Google Scholar 

  • Kaiya H, Miyazato M, Kangawa K, Peter RE, Unniappan S (2008) Ghrelin: a multifunctional hormone in non-mammalian vertebrates. Comp Biochem Physiol A Mol Integr Physiol 149(2):109–128

    Article  PubMed  Google Scholar 

  • Kawano H, Daikoku S, Saito S (1983) Location of thyrotropin-releasing hormone-like immunoreactivity in rat pancreas. Endocrinology 112(3):951–955

    Article  PubMed  CAS  Google Scholar 

  • Kelly OG, Melton DA (2000) Development of the pancreas in Xenopus laevis. Dev Dyn 218(4):615–627

    Article  PubMed  CAS  Google Scholar 

  • Kim SK, Rulifson EJ (2004) Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431:316–320

    Article  PubMed  CAS  Google Scholar 

  • Kim SK, Hebrok M, Melton DA (1997) Pancreas development in the chick embryo. Cold Spring Harb Symp Quant Biol 62:377–383

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi K, Syed AS (1981) Cell types of the endocrine pancreas in the shark Scyliorhinus stellaris as revealed by correlative light and electron microscopy. Cell Tissue Res 215(3):475–490

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Larsen MO, Rolin B (2004) Use of the Göttingen minipig as a model of diabetes, with special focus on type 1 diabetes research. ILAR J 45(3):303–313

    Article  PubMed  CAS  Google Scholar 

  • Lee JH, Ku SK, Lee HS, Kitagawa H (2003) An immunohistochemical study of endocrine cells in the pancreas of the Red-bellied frog (Bombina orientalis). Eur J Histochem 47(2):165–172

    PubMed  Google Scholar 

  • Leigh CM, Edwin N (1992) A light-microscopic immunocytochemical study of the endocrine pancreas in the Australian brush tailed possum (Trichosurus vulpecula). Eur J Histochem 36(2):237–241

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Masini MA (1988) Immunocytochemical localization of peptides in the endocrine pancreas of the snakes Vipera aspis and Natrix maura. Acta Histochem 84(2):111–119

    Article  PubMed  CAS  Google Scholar 

  • Mensah-Brown EP, Bailey TA, Pallot DJ, Garner A (2000) Peptidergic hormones and neuropeptides, and aminergic neurotransmitters of the pancreatic islets of the Houbara bustard (Chlamydotis undulata). J Anat 196(Pt 2):233–241

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Menzies BR, Shaw G, Fletcher TP, Renfree MB (2009) Early onset of ghrelin production in a marsupial. Mol Cell Endocrinol 299(2):266–273

    Article  PubMed  CAS  Google Scholar 

  • Michelmore AJ, Keegan DJ, Kramer B (1998) Rousettus aegyptiacus. Immunocytochemical identification of endocrine cells in the pancreas of the fruit bat. Gen Comp Endocrinol 110(3):319–325

    Article  PubMed  CAS  Google Scholar 

  • Nascimento AA, Sales A, Cardoso TR, Pinheiro NL, Mendes RM (2007) Immunocytochemical study of the distribution of endocrine cells in the pancreas of the Brazilian sparrow species Zonotrichia Capensis Subtorquata (Swaison, 1837). Braz J Biol 67(4):735–740

    Article  PubMed  CAS  Google Scholar 

  • Navarro MH, Lozano MT, Agulleiro B (2006) Ontogeny of the endocrine pancreatic cells of the gilthead sea bream, Sparus aurata (Teleost). Gen Comp Endocrinol 148(2):213–226

    Article  PubMed  CAS  Google Scholar 

  • Norris DO (1980) Vertebrate endocrinology. Lea and Febiger, Philadelphia

    Google Scholar 

  • Prado CL, Pugh-Bernard AE, Elghazi L, Sosa-Pineda B, Sussel L (2004) Ghrelin cells replace insulin-producing β cells in two mouse models of pancreas development. Proc Natl Acad Sci USA 101(9):2924–2929

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Reddy S, Bibby NJ, Fisher SL (1986) Elliott RB Immunolocalization of insulin, glucagon, pancreaticpolypeptide, and somatostatin in the pancreatic islets of the possum, Trichosurus vulpecula. Gen Comp Endocrinol 64(1):157–162

    Article  PubMed  CAS  Google Scholar 

  • Redecker P, Seipelt A, Jörns A, Bargsten G, Grube D (1992) The microanatomy of canine islets of Langerhans: implications for intra-islet regulation. Anat Embryol (Berl) 185(2):131–141

    Article  CAS  Google Scholar 

  • Reinecke M, Broger I, Brun R, Zapf J, Maake C (1995) Immunohistochemical localization of insulin-like growth factor I and II in the endocrine pancreas of birds, reptiles, and amphibia. Gen Comp Endocrinol 100(3):385–396

    Article  PubMed  CAS  Google Scholar 

  • Rhoten WB, Hall CE (1981) Four hormones in the pancreas of the lizard, anolis carolinensis. Anat Rec 199:89–97

    Article  PubMed  CAS  Google Scholar 

  • Rulifson EJ, Kim SK, Nusse R (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296:1118–1120

    Article  PubMed  CAS  Google Scholar 

  • Shimizu K, Kato Y, Shiratori K, Ding Y, Song Y, Furlanetto R, Chang TM, Watanabe S, Hayashi N, Kobayashi M, Chey WY (1998) Evidence for the existence of CCK-producing cells in rat pancreatic islets. Endocrinology 139(1):389–396

    PubMed  CAS  Google Scholar 

  • Simsek N, Ozüdoğru Z, Alabay B (2008) Immunohistochemical studies on the splenic lobe of the pancreas in young Japanese quails (Coturnix c. japonica). Dtsch Tierarztl Wochenschr 115(5):189–193

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Tsuruo Y, Hökfelt T, Visser TJ, Kimmel JR, Brown JC, Verhofstadt A, Walsh J (1988) TRH-like immunoreactivity in endocrine cells and neurons in the gastro-intestinal tract of the rat and guinea pig. Cell Tissue Res 253(2):347–356

    Article  PubMed  CAS  Google Scholar 

  • Van der Horst D (2003) Insect adipokinetic hormones: release and integration of flight energy metabolism. Comp Biochem Phys B 136:217–226

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wieczorek G, Pospischil A, Perentes E (1998) A comparative immunohistochemical study of pancreatic islets in laboratory animals (rats, dogs, minipigs, nonhuman primates). Exp Toxicol Pathol 50(3):151–172

    Article  PubMed  CAS  Google Scholar 

  • Wierup N, Svensson H, Mulder H, Sundler F (2002) The Ghrelin cell: a novel developmentally regulated islet cell in the human pancreas. Regul Pept 107(1–3):63–69

    Article  PubMed  CAS  Google Scholar 

  • Wierup N, Kuhar M, Nilsson BO, Mulder H, Ekblad E, Sundler F (2004) Cocaine-and amphetamine regulated transcript (CART) is expressed in several islet cell types during rat development. J Histochem Cytochem 52(2):169–177

    Article  PubMed  CAS  Google Scholar 

  • Youson JH (2007) Peripheral endocrine glands. I. The gastoenteropancreatic endocrine system and the thyroid gland. Fish Physiol Primit Fish 26:381–425

    Article  Google Scholar 

  • Youson JH, Al-Mahrouki AA (1999) Ontogenetic and phylogenetic development of the endocrine pancreas (islet organ) in fish. Gen Comp Endocrinol 116(3):303–335

    Article  PubMed  CAS  Google Scholar 

  • Youson JH, Al-Mahrouki AA, Amemiya Y, Graham LC, Montpetit CJ, Irwin DM (2006) The fish endocrine pancreas: review, new data, and future research directions in ontogeny and phylogeny. Gen Comp Endocrinol 148(2):105–115

    Article  PubMed  CAS  Google Scholar 

  • Yui R, Nagata Y, Fujita T (1988) Immunocytochemical studies on the islet and the gut of the arctic lamprey, Lampetra japonica. Arch Histol Cytol 51(1):109–119

    Article  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. 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 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

© 2015 Springer Science+Business Media Dordrecht

About this entry

Cite this entry

Heller, R.S. (2015). The Comparative Anatomy of Islets. In: Islam, M. (eds) Islets of Langerhans. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6686-0_2

Download citation

Publish with us

Policies and ethics