Comparison of histo- and organogenesis of human pancreas, white laboratory mouse and spiny mouse (Acomys)

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

The study of the embryonic development of the pancreas gives the opportunity to understand the mechanisms of organ regeneration in case of various pathologies. Worldwide research works, studying histo- and organogenesis of human pancreas, are based on data, received from model animals. Numerous processes of pancreatic development take several hours and remain unclear because white laboratory mouse has short gestation period. Spiny mouse (Acomys) has the prolonged prenatal period and can be a convenient model to study the stages of histo- and organogenesis of the pancreas. The review analyzed similarities and differences in the structure of human pancreas, white laboratory mouse and spiny mouse, the features of prenatal histo- and organogenesis of the pancreas, which should be considered in conducting and interpreting results of fundamental research, and possibility of using of spiny mice as a model animal to study embryonic development and pathology of the pancreas.

Full Text

Restricted Access

About the authors

K. N. Sultanova

Kazan (Volga region) Federal University

Author for correspondence.
Email: kasana555_07@mail.ru
Russian Federation, Kazan

A. A. Titova

Kazan (Volga region) Federal University

Email: kasana555_07@mail.ru
Russian Federation, Kazan

A. S. Plushkina

Kazan (Volga region) Federal University

Email: kasana555_07@mail.ru
Russian Federation, Kazan

D. I. Andreeva

Kazan (Volga region) Federal University

Email: kasana555_07@mail.ru
Russian Federation, Kazan

A. P. Kiyasov

Kazan (Volga region) Federal University

Email: kasana555_07@mail.ru
Russian Federation, Kazan

References

  1. Zhou Q., Melton D.A. Pancreas regeneration. Nature 2018; 557(7705): 351–8.
  2. Dhawan S., Georgia S., Bhushan A. Formation and regeneration of the endocrine pancreas. Curr. Opin. Cell Biol. 2007; 19(6): 634–45.
  3. Мирецкая Е.И. Биомедицинские исследования на человеке: правовые и морально-этические проблемы. Юридическая наука и практика: Вестник Нижегородской академии МВД России 2014; 2(26): 235–7. [Miretskaya E.I. Biomedical researches on the person: legal and moral and ethical problems. Legal science and practice: Journal of the Nizhny Novgorod Academy of the Ministry of Internal Affairs of Russia 2014; 2(26): 235–7].
  4. Haughton C.L., Gawriluk T.R., Seifert A.W. The biology and husbandry of the african spiny mouse (Acomys cahirinus) and the research uses of a laboratory colony. J.Am. Assoc. Lab. Anim. Sci. 2016; 55(1): 9–17.
  5. Lamers W.H., Mooren P.G., Oosterhuis W. et al. The relation between the developmental timing of birth and developmental increases in urea cycle enzymes. Adv. Exp. Med. Biol. 1982; 153: 229–40.
  6. Shafrir E., Ziv E., Kalman R. Nutritionally induced diabetes in desert rodents as models of type 2 diabetes: Acomys cahirinus (spiny mice) and Psammomys obesus (desert gerbil). ILAR J. 2006; 47(3): 212–24.
  7. de Gasparo M. Accumulation of pancreas-specific products during organogenesis of Acomys cahirinus. Gen. Comp. Endocrinol. 1980; 41(4): 499–505.
  8. Rahier J., Wallon J., Henquin J.C. Cell populations in the endocrine pancreas of human neonates and infants. Diabetologia 1981; 20(5): 540–6.
  9. In't Veld P., Marichal M. Microscopic anatomy of the human islet of Langerhans. Adv. Exp. Med. Biol. 2010; 654: 1–19.
  10. Watanabe T., Yaegashi H., Koizumi M. et al. The lobular architecture of the normal human pancreas: a computer-assisted three-dimensional reconstruction study. Pancreas 1997; 15(1): 48–52.
  11. El-Gohary Y., Sims-Lucas S., Lath N. et al. Three-dimensional analysis of the islet vasculature. Anat. Rec. (Hoboken) 2012; 295(9): 1473–81.
  12. Saisho Y., Butler A.E., Manesso E. et al. β-cell mass and turnover in humans: effects of obesity and aging. Diabetes Care 2013; 36(1): 111–7.
  13. Kim A., Miller K., Jo J. et al. Islet architecture: a comparative study. Islets 2009; 1(2): 129–36.
  14. Andralojc K.M., Mercalli A., Nowak K.W. et al. Ghrelin-producing epsilon cells in the developing and adult human pancreas. Diabetologia 2009; 52(3): 486–93.
  15. Merkwitz C., Blaschuk O.W., Schulz A. et al. The ductal origin of structural and functional heterogeneity between pancreatic islets. Prog. Histochem. Cytochem. 2013; 48(3): 103–40.
  16. Dolenšek J., Rupnik M.S., Stožer A. Structural similarities and differences between the human and the mouse pancreas. Islets 2015; 7(1): e1024405.
  17. Erlandsen S.L., Hegre O.D., Parsons J.A. et al. Pancreatic islet cell hormones distribution of cell types in the islet and evidence for the presence of somatostatin and gastrin within the D cell. J. Histochem. Cytochem. 1976; 24(7): 883–97.
  18. Grube D., Bohn R. The microanatomy of human islets of Langerhans, with special reference to somatostatin (D-) cells. Arch. Histol. Jpn. 1983; 46(3): 327–53.
  19. Cabrera O., Berman D.M., Kenyon N.S. et al. The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. PNAS USA 2006; 103(7): 2334–9.
  20. Bunnag S.C., Bunnag S., Warner N.E. Microcirculation in the islets of Langerhans of the mouse. Anat. Rec. 1963; 146: 117–23.
  21. Liu X.Y., Xue L., Zheng X. et al. Pancreas transplantation in the mouse. Hepatobiliary Pancreat. Dis. Int. 2010; 9(3): 254–8.
  22. Watanabe S., Abe K., Anbo Y. et al. Changes in the mouse exocrine pancreas after pancreatic duct ligation: a qualitative and quantitative histological study. Arch. Histol. Cytol. 1995; 58(3): 365–74.
  23. Villasenor A., Chong D.C., Henkemeyer M. et al. Epithelial dynamics of pancreatic branching morphogenesis. Development 2010; 137(24): 4295–305.
  24. Hörnblad A., Cheddad A., Ahlgren U. An improved protocol for optical projection tomography imaging reveals lobular heterogeneities in pancreatic islet and β-cell mass distribution. Islets 2011; 3(4): 204–8.
  25. Pfeifer C.R., Shomorony A., Aronova M.A. et al. Quantitative analysis of mouse pancreatic islet architecture by serial block-face SEM. J. Struct. Biol. 2015; 189(1): 44–52.
  26. Steiner D.J., Kim A., Miller K. et al. Pancreatic islet plasticity: interspecies comparison of islet architecture and composition. Islets 2010; 2(3): 135–45.
  27. Kilimnik G., Zhao B., Jo J. et al. Altered islet composition and disproportionate loss of large islets in patients with type 2 diabetes. PLoS One 2011; 6(11): e27445.
  28. Wang X., Misawa R., Zielinski M.C. et al. Regional differences in islet distribution in the human pancreas-preferential beta-cell loss in the head region in patients with type 2 diabetes. PLoS One 2013; 8(6): e67454.
  29. Henquin J.C., Rahier J. Pancreatic alpha cell mass in European subjects with type 2 diabetes. Diabetologia 2011; 54(7): 1720–5.
  30. Rorsman P., Braun M. Regulation of insulin secretion in human pancreatic islets. Annu. Rev. Physiol. 2013; 75: 155–79.
  31. Murakami T., Hitomi S., Ohtsuka A. et al. Pancreatic insulo-acinar portal systems in humans, rats, and some other mammals: scanning electron microscopy of vascular casts. Microsc. Res. Tech. 1997; 37(5–6): 478–88.
  32. Gustavsen C.R., Kvicerova J., Dickinson H. et al. Acomys, the closest relatives to Gerbils, do express Pdx-1 protein and have similar islet morphology to Gerbils. Islets 2009; 1(3): 191–7.
  33. Gonet A.E., Stauffacher W., Pictet R. et al. Obesity and diabetes mellitus with striking congenital hyperplasia of the islets of langerhans in spiny mice (Acomys Cahirinus): I. Histological findings and preliminary metabolic observations. Diabetologia 1966; 1(3–4): 162–71.
  34. Andrei S.R., Gannon M. Embryonic development of the endocrine pancreas. Transplantation, Bioengineering and regeneration of endocrine pancreas 2020; 2: 171–82.
  35. Jørgensen M.C., Ahnfelt-Rønne J., Hald J. et al. An illustrated review of early pancreas development in the mouse. Endocr. Rev. 2007; 28(6): 685–705.
  36. Piper K., Brickwood S., Turnpenny L.W. et al. Beta cell differentiation during early human pancreas development. J. Endocrinol. 2004; 181(1): 11–23.
  37. Scharfmann R. Control of early development of the pancreas in rodents and humans: implications of signals from the mesenchyme. Diabetologia 2000; 43(9): 1083–92.
  38. Murtaugh L.C. Pancreas and beta-cell development: from the actual to the possible. Development 2007; 134(3): 427–38.
  39. Pan F.C., Wright C. Pancreas organogenesis: from bud to plexus to gland. Dev. Dyn. 2011; 240(3): 530–65.
  40. Jennings R.E., Berry A.A., Kirkwood-Wilson R. et al. Development of the human pancreas from foregut to endocrine commitment. Diabetes 2013; 62(10): 3514–22.
  41. Like A.A., Orci L. Embryogenesis of the human pancreatic islets: a light and electron microscopic study. Diabetes 1972; 21(2): 511–34.
  42. Калигин М.С., Гумерова А.А., Титова М.А. и соавт. C-kit маркёр стволовых клеток эндокриноцитов поджелудочной железы человека. Морфология 2011; 140(4): 32–7 [Kaligin M.S., Gumerova A.A., Titova M.A. et al. C-kit is a marker of human pancreatic endocrinocyte stem cells. Morfology 2011; 140(4): 32–7].
  43. Krivova Y.S., Proshchina A.E., Barabanov V.M. et al. Development of the islets of Langerhans in the human fetal pancreas. In: Satou A., Nakamura H., editors. Pancreas: Anatomy, Diseases and Health Implications. New York: Nova Science Publishers; 2012: 53–88.
  44. Brissova M., Fowler M.J., Nicholson W.E. et al. Assessment of human pancreatic islet architecture and composition by laser scanning confocal microscopy. J. Histochem. Cytochem. 2005; 53(9): 1087–97.
  45. Jeon J., Correa-Medina M., Ricordi C. et al. Endocrine cell clustering during human pancreas development. J. Histochem. Cytochem. 2009; 57(9): 811–24.
  46. Pan F.C., Brissova M. Pancreas development in humans. Curr. Opin. Endocrinol. Diabetes Obes. 2014; 21(2): 77–82.
  47. Wessells N.K., Cohen J.H. Early pancreas organogenesis: morphogenesis, tissue interactions, and mass effects. Dev. Biol. 1967; 15(3): 237–70.
  48. Spooner B.S., Walther B.T., Rutter W.J. The development of the dorsal and ventral mammalian pancreas in vivo and in vitro. J. Cell Biol. 1970; 47(1): 235–46.
  49. Pictet R.L., Clark W.R., Williams R.H. et al. An ultrastructural analysis of the developing embryonic pancreas. Dev. Biol. 1972; 29(4): 436–67.
  50. Rutter W.J., Kemp J.D., Bradshaw W.S. et al. Regulation of specific protein synthesis in cytodifferentiation. J. Cell. Physiol. 1968; 72(2) Suppl 1: 1–18.
  51. Teitelman G., Alpert S., Polak J.M. et al. Precursor cells of mouse endocrine pancreas coexpress insulin, glucagon and the neuronal proteins tyrosine hydroxylase and neuropeptide Y, but not pancreatic polypeptide. Development 1993; 118(4): 1031–9.
  52. Herrera P.L., Huarte J., Sanvito F. et al. Embryogenesis of the murine endocrine pancreas; early expression of pancreatic polypeptide gene. Development 1991; 113(4): 1257–65.
  53. Heller R.S., Jenny M., Collombat P. et al. Genetic determinants of pancreatic epsilon-cell development. Dev. Biol. 2005; 286(1): 217–24.
  54. Upchurch B.H., Aponte G.W., Leiter A.B. Expression of peptide YY in all four islet cell types in the developing mouse pancreas suggests a common peptide YY-producing progenitor. Development 1994; 120(2): 245–52.
  55. Apelqvist A., Li H., Sommer L. et al. Notch signalling controls pancreatic cell differentiation. Nature 1999; 400(6747): 877–81.
  56. Gittes G.K., Rutter W.J. Onset of cell-specific gene expression in the developing mouse pancreas. PNAS USA 1992; 89(3): 1128–32.
  57. Chiang M.K., Melton D.A. Single-cell transcript analysis of pancreas development. Dev. Cell 2003; 4(3): 383–93.
  58. Peterka M., Lesot H., Peterková R. Body weight in mouse embryos specifies staging of tooth development. Connect. Tissue Res. 2002; 43(2–3): 186–90.
  59. Dickinson H., Walker D.W., Cullen-McEwen L. et al. The spiny mouse (Acomys cahirinus) completes nephrogenesis before birth. Am.J. Physiol. Renal Physiol. 2005; 289(2): F273–9.
  60. Ryökkynen A., Kukkonen J.V., Nieminen P. Effects of dietary genistein on mouse reproduction, postnatal development and weight-regulation. Anim. Reprod. Sci. 2006; 93(3–4): 337–48.
  61. Santiago S.E., Huffman K.J. Postnatal effects of prenatal nicotine exposure on body weight, brain size and cortical connectivity in mice. Neurosci. Res. 2012; 73(4): 282–91.
  62. Lamers W.H., Mooren P.G., Charles R. Perinatal development of the small intestine and pancreas in rat and spiny mouse. Its relation to altricial and precocial timing of birth. Biol. Neonate 1985; 47(3): 153–62.
  63. Pedersen J.K., Nelson S.B., Jorgensen M.C. et al. Endodermal expression of Nkx6 genes depends differentially on Pdx1. Dev. Biol. 2005; 288(2): 487–501.
  64. Zaret K.S., Grompe M. Generation and regeneration of cells of the liver and pancreas. Science 2008; 322(5907): 1490–4.
  65. Zorn A.M., Wells J.M. Vertebrate endoderm development and organ formation. Annu. Rev. Cell Dev. Biol. 2009; 25: 221–51.
  66. Sakhneny L., Khalifa-Malka L., Landsman L. Pancreas organogenesis: Approaches to elucidate the role of epithelial-mesenchymal interactions. Semin. Cell Dev. Biol. 2019; 92: 89–96.
  67. Ohlsson H., Karlsson K., Edlund T. IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J. 1993; 12(11): 4251–9.
  68. Ahlgren U., Jonsson J., Edlund H. The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice. Development 1996; 122(5): 1409–16.
  69. Li H., Arber S., Jessell T.M. et al. Selective agenesis of the dorsal pancreas in mice lacking homeobox gene Hlxb9. Nat. Genet. 1999; 23(1): 67–70.
  70. Jonsson J., Carlsson L., Edlund T. et al. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 1994; 371(6498): 606–9.
  71. Gu G., Dubauskaite J., Melton D.A. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002; 129(10): 2447–57.
  72. Dufort D., Schwartz L., Harpal K. et al. The transcription factor HNF3beta is required in visceral endoderm for normal primitive streak morphogenesis. Development 1998; 125(16): 3015–25.
  73. Harrison K.A., Thaler J., Pfaff S.L. et al. Pancreas dorsal lobe agenesis and abnormal islets of Langerhans in Hlxb9-deficient mice. Nat. Genet. 1999; 23(1): 71–5.
  74. Grapin-Botton A., Majithia A.R., Melton D.A. Key events of pancreas formation are triggered in gut endoderm by ectopic expression of pancreatic regulatory genes. Genes Dev. 2001; 15(4): 444–54.
  75. Jacquemin P., Lemaigre F.P., Rousseau G.G. The Onecut transcription factor HNF-6 (OC-1) is required for timely specification of the pancreas and acts upstream of Pdx-1 in the specification cascade. Dev. Biol. 2003; 258(1): 105–16.
  76. Bort R., Martinez-Barbera J.P., Beddington R.S. et al. Hex homeobox gene-dependent tissue positioning is required for organogenesis of the ventral pancreas. Development 2004; 131(4): 797–806.
  77. Haumaitre C., Barbacci E., Jenny M. et al. Lack of TCF2/vHNF1 in mice leads to pancreas agenesis. PNAS USA 2005; 102(5): 1490–5.
  78. Poll A.V., Pierreux C.E., Lokmane L. et al. A vHNF1/TCF2-HNF6 cascade regulates the transcription factor network that controls generation of pancreatic precursor cells. Diabetes 2006; 55(1): 61–9.
  79. Guz Y., Montminy M.R., Stein R. et al. Expression of murine STF-1, a putative insulin gene transcription factor, in beta cells of pancreas, duodenal epithelium and pancreatic exocrine and endocrine progenitors during ontogeny. Development 1995; 121(1): 11–8.
  80. Miller C.P., McGehee R.E., Habener J.F. IDX-1: a new homeodomain transcription factor expressed in rat pancreatic islets and duodenum that transactivates the somatostatin gene. EMBO J. 1994; 13(5): 1145–56.
  81. Offield M.F., Jetton T.L., Labosky P.A. et al. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 1996; 122(3): 983–95.
  82. Jensen J., Heller R.S., Funder-Nielsen T. et al. Independent development of pancreatic alpha- and beta-cells from neurogenin3-expressing precursors: a role for the notch pathway in repression of premature differentiation. Diabetes 2000; 49(2): 163–76.
  83. Jennings R.E., Scharfmann R., Staels W. Transcription factors that shape the mammalian pancreas. Diabetologia 2020; 63(10): 1974–80.
  84. Gradwohl G., Dierich A., LeMeur M. et al. Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. PNAS USA 2000; 97(4): 1607–11.
  85. Schwitzgebel V.M., Scheel D.W., Conners J.R. et al. Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 2000; 127(16): 3533–42.
  86. Sommer L., Ma Q., Anderson D.J. Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol. Cell. Neurosci. 1996; 8(4): 221–41.
  87. Lee J.C., Smith S.B., Watada H. et al. Regulation of the pancreatic pro-endocrine gene neurogenin3. Diabetes 2001; 50(5): 928–36.
  88. Salisbury R.J., Blaylock J., Berry A.A. et al. The window period of NEUROGENIN3 during human gestation. Islets 2014; 6(3): e954436.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2022 Eco-Vector


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: 

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies