Comparative aspects of rodent and nonrodent animal models for mechanistic and translational diabetes research

Theriogenology

Volumn 86, Issue 1, 2016, Pages 406-421

  Renner, Simone ^a,b   Dobenecker, Britta ^a   Blutke, Andreas ^a   Zöls, Susanne ^a   Wanke, Rüdiger ^a   Ritzmann, Mathias ^a   Wolf, Eckhard ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Animal model; Diabetes; Genetic modification; High fat diet; Metabolic syndrome; Pig

Indexed keywords

ANTIDIABETIC AGENT;

ANIMAL; BIOETHICS; DIABETES MELLITUS; DISEASE MODEL; HUMAN; MEDICAL RESEARCH; PROCEDURES; RODENT;

ANIMALS; BIOETHICS; BIOMEDICAL RESEARCH; DIABETES MELLITUS; DISEASE MODELS, ANIMAL; HUMANS; HYPOGLYCEMIC AGENTS; RODENTIA;

EID: 84969961943     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2016.04.055     Document Type: Review

References (204)

1. IDF Diabetes Atlas 2013, Federation ID, online available at. http://www.idf.org/diabetesatlas, Sixth edition.
2. Ng M., Fleming T., Robinson M., Thomson B., Graetz N., Margono C., et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014, 384:766-781.
3. Classification and diagnosis of diabetes. Diabetes Care 2015, 38:S8-S16. American Diabetes Association.
4. Bellamy L., Casas J.P., Hingorani A.D., Williams D. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet 2009, 373:1773-1779.
5. Hay M., Thomas D.W., Craighead J.L., Economides C., Rosenthal J. Clinical development success rates for investigational drugs. Nat Biotechnol 2014, 32:40-51.
6. Wolf E., Braun-Reichhart C., Streckel E., Renner S. Genetically engineered pig models for diabetes research. Transgenic Res 2014, 23:27-38.
7. Ellegaard B. http://www.minipigs.dk/.
8. Webster J., Bollen P., Grimm H., Jennings M. Steering Group of the RETHINK Project, Ethical implications of using the minipig in regulatory toxicology studies. J Pharmacol Toxicol Methods 2010, 62:160-166.
9. Rehg J.E., Toth L.A. Rodent quarantine programs: purpose, principles, and practice. Lab Anim Sci 1998, 48:438-447.
10. Kolstoe E.M., Iversen T., Ostensvik O., Abdelghani A., Secic I., Nesbakken T. Specific pathogen-free pig herds also free from Campylobacter?. Zoonoses Public Health 2015, 62:125-130.
11. Morton W.R., Agy M.B., Capuano S.V., Grant R.F. Specific pathogen-free macaques: definition, history, and current production. ILAR J 2008, 49:137-144.
12. Abee C.R., Mansfield K., Tardif S., Morris T. Nonhuman Primates in Biomedical Research - Biology and Management 2012, Academic Press, New York, NY.
13. Hedrich H.J. The Laboratory Mouse 2012, Academic Press, Cambridge, Massachusetts, USA. Second edition.
14. Suckow M.A., W S.H., Franklin L.C. The Laboratory Rat 2000, Academic Press, Cambridge, Massachusetts, USA. Second edition.
15. Suckow M.A. The Laboratory Rabbit, Guinea Pig, Hamster, and Other Rodents (American College of Laboratory Animal Medicine) 2012, Academic Press, Cambridge, Massachusetts, USA.
16. Tumbleson M. Swine in Biomedical Research 1986, Plenum Publishing Corporation, New York City, USA.
17. Wolfe-Coote S. The Laboratory Primate 2005, Elsevier, Amsterdam, The Netherlands.
18. de Angelis M.H., Nicholson G., Selloum M., White J.K., Morgan H., Ramirez-Solis R., et al. Analysis of mammalian gene function through broad-based phenotypic screens across a consortium of mouse clinics. Nat Genet 2015, 47:969-978.
19. Sasaki E. Prospects for genetically modified non-human primate models, including the common marmoset. Neurosci Res 2015, 93:110-115.
20. Pond W.G., M H.J. Biology of the domestic pig-General characteristics 2001, 15-20. Cornell University Press, Ithaca, USA.
21. Fernstrom A.L., Fredlund H., Spangberg M., Westlund K. Positive reinforcement training in rhesus macaques-training progress as a result of training frequency. Am J Primatol 2009, 71:373-379.
22. Bliss-Moreau E., Theil J.H., Moadab G. Efficient cooperative restraint training with rhesus macaques. J Appl Anim Welfare Sci 2013, 16:98-117.
23. Coleman K., Pranger L., Maier A., Lambeth S.P., Perlman J.E., Thiele E., et al. Training rhesus macaques for venipuncture using positive reinforcement techniques: a comparison with chimpanzees. J Am Assoc Lab Anim Sci 2008, 47:37-41.
24. Sengupta P. The laboratory rat: relating its age with Human's. Int J Prev Med 2013, 4:624-630.
25. NC3Rs (National Centre for the Replacement RaRoAiR. The Macaque Website. http://www.nc3rs.org.uk/macaques/.
26. Fischer B., Chavatte-Palmer P., Viebahn C., Navarrete Santos A., Duranthon V. Rabbit as a reproductive model for human health. Reproduction 2012, 144:1-10.
27. Hofmann A., Kessler B., Ewerling S., Weppert M., Vogg B., Ludwig H., et al. Efficient transgenesis in farm animals by lentiviral vectors. EMBO Rep 2003, 4:1054-1060.
28. Phelps C.J., Koike C., Vaught T.D., Boone J., Wells K.D., Chen S.H., et al. Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003, 299:411-414.
29. Klymiuk N., Bocker W., Schonitzer V., Bahr A., Radic T., Frohlich T., et al. First inducible transgene expression in porcine large animal models. FASEB J 2012, 26:1086-1099.
30. Carlson D.F., Fahrenkrug S.C., Hackett P.B. Targeting DNA with fingers and TALENs. Mol Ther Nucleic Acids 2012, 1:e3.
31. Hauschild J., Petersen B., Santiago Y., Queisser A.L., Carnwath J.W., Lucas-Hahn A., et al. Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc Natl Acad Sci U S A 2011, 108:12013-12017.
32. Hai T., Teng F., Guo R., Li W., Zhou Q. One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res 2014, 24:372-375.
33. Sachs D.H., Leight G., Cone J., Schwarz S., Stuart L., Rosenberg S. Transplantation in miniature swine. I. Fixation of the major histocompatibility complex. Transplantation 1976, 22:559-567.
34. van der Laan J.W., Brightwell J., McAnulty P., Ratky J., Stark C. Regulatory acceptability of the minipig in the development of pharmaceuticals, chemicals and other products. J Pharmacol Toxicol Methods 2010, 62:184-195. Steering Group of the RP.
35. Ludwig B., Ludwig S. Transplantable bioartificial pancreas devices: current status and future prospects. Langenbecks Arch Surg 2015, 400:531-540.
36. Escareno C.E., Azagury D.E., Flint R.S., Nedder A., Thompson C.C., Lautz D.B. Establishing a reproducible large animal survival model of laparoscopic Roux-en-Y gastric bypass. Surg Obes Relat Dis 2012, 8:764-769.
37. Dixon J.A., Spinale F.G. Large animal models of heart failure: a critical link in the translation of basic science to clinical practice. Circ Heart Fail 2009, 2:262-271.
38. Hoyer C., Gass N., Weber-Fahr W., Sartorius A. Advantages and challenges of small animal magnetic resonance imaging as a translational tool. Neuropsychobiology 2014, 69:187-201.
39. Laurent D., Vinet L., Lamprianou S., Daval M., Filhoulaud G., Ktorza A., et al. Pancreatic beta-cell imaging in humans: fiction or option?. Diabetes Obes Metab 2015, 69:187-201.
40. Renner S., Braun-Reichhart C., Blutke A., Herbach N., Emrich D., Streckel E., et al. Permanent neonatal diabetes in INS(C94Y) transgenic pigs. Diabetes 2013, 62:1505-1511.
41. Renner S., Fehlings C., Herbach N., Hofmann A., von Waldthausen D.C., Kessler B., et al. Glucose intolerance and reduced proliferation of pancreatic beta-cells in transgenic pigs with impaired glucose-dependent insulinotropic polypeptide function. Diabetes 2010, 59:1228-1238.
42. Lee L., Alloosh M., Saxena R., Van Alstine W., Watkins B.A., Klaunig J.E., et al. Nutritional model of steatohepatitis and metabolic syndrome in the Ossabaw miniature swine. Hepatology 2009, 50:56-67.
43. Rozman J., Rathkolb B., Neschen S., Fuchs H., Gailus-Durner V., Klingenspor M., et al. Glucose tolerance tests for systematic screening of glucose homeostasis in mice. Curr Protoc Mouse Biol 2015, 5:65-84.
44. Wolczuk K., Wilczynska B., Jaroszewska M., Kobak J. Morphometric characteristics of the small and large intestines of Mus musculus during postnatal development. Folia Morphol 2011, 70:252-259.
45. Permezel N.C., Webling D.D. The length and mucosal surface area of the small and large gut in young rats. J Anat 1971, 108:295-296.
46. Hounnou G., Destrieux C., Desme J., Bertrand P., Velut S. Anatomical study of the length of the human intestine. Surg Radiol Anat 2002, 24:290-294.
47. Dressman J.B., Thelen K., Willmann S. An update on computational oral absorption simulation. Expert Opin Drug Metab Toxicol 2011, 7:1345-1364.
48. Bahr R., Flach A. Morphological and functional adaptation after massive resection of the small intestine: experiments using minipigs of the Gottingen strain. Prog Pediatr Surg 1978, 12:107-142.
49. Glodek P., Oldigs B. Das Göttingen Minischwein 1981, Paul Parey, Berlin.
50. Kühn U. Vergleichende anatomische Untersuchungen des Darmtraktes und des darmassoziierten lymphatischen Gewebes (GALT) bei alten Hausschweinerassen und einer modernen Fleischrasse 2001, School Vet Med Hannover: Tierärztlichen Hochschule Hannover, Hannover, Germany.
51. Kurihara-Bergstrom T., Woodworth M., Feisullin S., Beall P. Characterization of the Yucatan miniature pig skin and small intestine for pharmaceutical applications. Lab Anim Sci 1986, 36:396-399.
52. Dressman J.B., Yamada K. Animal models for oral drug absorption. Drugs Pharm Sci 1991, 48:235-266.
53. Dahlhoff M., Horst D., Gerhard M., Kolligs F.T., Wolf E., Schneider M.R. Betacellulin stimulates growth of the mouse intestinal epithelium and increases adenoma multiplicity in Apc+/Min mice. FEBS Lett 2008, 582:2911-2915.
54. Kararli T.T. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos 1995, 16:351-380.
55. Stevens C.E., Hume I.D. Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 1998, 78:393-427.
56. Padmanabhan P., Grosse J., Asad A.B., Radda G.K., Golay X. Gastrointestinal transit measurements in mice with 99mTc-DTPA-labeled activated charcoal using NanoSPECT-CT. EJNMMI Res 2013, 3:60.
57. Ghoshal U.C., Sengar V., Srivastava D. Colonic transit study technique and interpretation: can these be uniform globally in different populations with non-uniform colon transit time?. J Neurogastroenterol Motil 2012, 18:227-228.
58. Kim S.K. Small intestine transit time in the normal small bowel study. Am J Roentgenol Ther Nucl Med 1968, 104:522-524.
59. Mercier G.T., Nehete P.N., Passeri M.F., Nehete B.N., Weaver E.A., Templeton N.S., et al. Oral immunization of rhesus macaques with adenoviral HIV vaccines using enteric-coated capsules. Vaccine 2007, 25:8687-8701.
60. Davis S.S., Illum L., Hinchcliffe M. Gastrointestinal transit of dosage forms in the pig. J Pharm Pharmacol 2001, 53:33-39.
61. Adkin D.A., Davis S.S., Sparrow R.A., Huckle P.D., Phillips A.J., Wilding I.R. The effects of pharmaceutical excipients on small intestinal transit. Br J Clin Pharmacol 1995, 39:381-387.
62. Graff J., Brinch K., Madsen J.L. Gastrointestinal mean transit times in young and middle-aged healthy subjects. Clin Physiol 2001, 21:253-259.
63. Wilfart A., Montagne L., Simmins H., Noblet J., Milgen J. Digesta transit in different segments of the gastrointestinal tract of pigs as affected by insoluble fibre supplied by wheat bran. Br J Nutr 2007, 98:54-62.
64. Gad S.C. Animal Models in Toxicology 2015, Taylor & Francis Inc., Abingdon, United Kingdom. Third edition.
65. McConnell E.L., Basit A.W., Murdan S. Measurements of rat and mouse gastrointestinal pH, fluid and lymphoid tissue, and implications for in-vivo experiments. J Pharm Pharmacol 2008, 60:63-70.
66. Chen E.P., Mahar Doan K.M., Portelli S., Coatney R., Vaden V., Shi W. Gastric pH and gastric residence time in fasted and fed conscious cynomolgus monkeys using the Bravo pH system. Pharm Res 2008, 25:123-134.
67. Merchant H.A., McConnell E.L., Liu F., Ramaswamy C., Kulkarni R.P., Basit A.W., et al. Assessment of gastrointestinal pH, fluid and lymphoid tissue in the guinea pig, rabbit and pig, and implications for their use in drug development. Eur J Pharm Sci 2011, 42:3-10.
68. Oberle R.L., Das H. Variability in gastric pH and delayed gastric emptying in Yucatan miniature pigs. Pharm Res 1994, 11:592-594.
69. Nguyen T.L., Vieira-Silva S., Liston A., Raes J. How informative is the mouse for human gut microbiota research?. Dis Models Mech 2015, 8:1-16.
70. Ley R.E., Backhed F., Turnbaugh P., Lozupone C.A., Knight R.D., Gordon J.I. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 2005, 102:11070-11075.
71. McKenna P., Hoffmann C., Minkah N., Aye P.P., Lackner A., Liu Z., et al. The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog 2008, 4:e20.
72. Jung E.C., Maibach H.I. Animal models for percutaneous absorption. J Appl Toxicol 2015, 35:1-10.
73. Schneider M.R., Wolf E. Genetically engineered pigs as investigative and translational models in dermatology. Br J Dermatol 2016, 174:237-239.
74. Bartelt A., Heeren J. Adipose tissue browning and metabolic health. Nat Rev Endocrinol 2014, 10:24-36.
75. Jastroch M., Andersson L. When pigs fly, UCP1 makes heat. Mol Metab 2015, 4:359-362.
76. Larsen M.O., Juhl C.B., Porksen N., Gotfredsen C.F., Carr R.D., Ribel U., et al. Beta-cell function and islet morphology in normal, obese, and obese beta-cell mass-reduced Gottingen minipigs. Am J Physiol Endocrinol Metab 2005, 288:E412-E421.
77. Schneider M.R., Dahlhoff M., Herbach N., Renner-Mueller I., Dalke C., Puk O., et al. Betacellulin overexpression in transgenic mice causes disproportionate growth, pulmonary hemorrhage syndrome, and complex eye pathology. Endocrinology 2005, 146:5237-5246.
78. Gotfredsen C.F., Molck A.M., Thorup I., Nyborg N.C., Salanti Z., Knudsen L.B., et al. The human GLP-1 analogs liraglutide and semaglutide: absence of histopathological effects on the pancreas in nonhuman primates. Diabetes 2014, 63:2486-2497.
79. Caglar V., Kumral B., Uygur R., Alkoc O.A., Ozen O.A., Demirel H. Study of volume, weight and size of normal pancreas, spleen and kidney in adults autopsies. Forensic Med Anat Res 2014, 2:63-69.
80. Ferrer J., Scott W.E., Weegman B.P., Suszynski T.M., Sutherland D.E., Hering B.J., et al. Pig pancreas anatomy: implications for pancreas procurement, preservation, and islet isolation. Transplantation 2008, 86:1503-1510.
81. Bertelli E., Di Gregorio F., Bertelli L., Civeli L., Mosca S. The arterial blood supply of the pancreas: a review. III. The inferior pancreaticoduodenal artery. An anatomical review and a radiological study. Surg Radiol Anat 1996, 18:67-74.
82. Watanabe S., Abe K., Anbo Y., Katoh H. Changes in the mouse exocrine pancreas after pancreatic duct ligation: a qualitative and quantitative histological study. Arch Histol Cytol 1995, 58:365-374.
83. Watanabe T., Yaegashi H., Koizumi M., Toyota T., Takahashi T. The lobular architecture of the normal human pancreas: a computer-assisted three-dimensional reconstruction study. Pancreas 1997, 15:48-52.
84. Wu C., Shea J.E. Structural similarities and differences between amyloidogenic and non-amyloidogenic islet amyloid polypeptide (IAPP) sequences and implications for the dual physiological and pathological activities of these peptides. PLoS Comput Biol 2013, 9:e1003211.
85. Herbach N., Goeke B., Schneider M., Hermanns W., Wolf E., Wanke R. Overexpression of a dominant negative GIP receptor in transgenic mice results in disturbed postnatal pancreatic islet and beta-cell development. Regul Pept 2005, 125:103-117.
86. Saito K., Iwama N., Takahashi T. Morphometrical analysis on topographical difference in size distribution, number and volume of islets in the human pancreas. Tohoku J Exp Med 1978, 124:177-186.
87. 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, 50:151-172.
88. Kobayashi T., Nakanishi K., Nakase H., Kajio H., Okubo M., Murase T., et al. In situ characterization of islets in diabetes with a mitochondrial DNA mutation at nucleotide position 3243. Diabetes 1997, 46:1567-1571.
89. Larsen M.O., Gotfredsen C.F., Wilken M., Carr R.D., Porksen N., Rolin B. Loss of beta-cell mass leads to a reduction of pulse mass with normal periodicity, regularity and entrainment of pulsatile insulin secretion in Gottingen minipigs. Diabetologia 2003, 46:195-202.
90. Cabrera O., Berman D.M., Kenyon N.S., Ricordi C., Berggren P.O., Caicedo A. The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. Proc Natl Acad Sci U S A 2006, 103:2334-2339.
91. Brissova M., Fowler M.J., Nicholson W.E., Chu A., Hirshberg B., Harlan D.M., et al. Assessment of human pancreatic islet architecture and composition by laser scanning confocal microscopy. J Histochem Cytochem 2005, 53:1087-1097.
92. Kharouta M., Miller K., Kim A., Wojcik P., Kilimnik G., Dey A., et al. No mantle formation in rodent islets-the prototype of islet revisited. Diabetes Res Clin Pract 2009, 85:252-257.
93. Rhoten W.B. Somatostatin-containing and other endocrine cells in the pancreas of the spectacled caiman. Acta Anat (Basel) 1987, 129:257-261.
94. Krickhahn M., Buhler C., Meyer T., Thiede A., Ulrichs K. The morphology of islets within the porcine donor pancreas determines the isolation result: successful isolation of pancreatic islets can now be achieved from young market pigs. Cell Transplant 2002, 11:827-838.
95. Ulrichs K., Eber S., Schneiker B., Gahn S., Strauss A., Moskalenko V., et al. Isolation of porcine pancreatic islets for xenotransplantation. Methods Mol Biol 2012, 885:213-232.
96. Feldman J.M., Chapman B. Preparation of islets of Langerhans from rabbits and hamsters by the collagenase digestion technique. Acta Diabetol Lat 1975, 12:208-218.
97. Rahier J., Wallon J., Henquin J.C. Cell populations in the endocrine pancreas of human neonates and infants. Diabetologia 1981, 20:540-546.
98. Saisho Y., Butler A.E., Manesso E., Elashoff D., Rizza R.A., Butler P.C. Beta-cell mass and turnover in humans: effects of obesity and aging. Diabetes Care 2013, 36:111-117.
99. Maclean N., Ogilvie R.F. Quantitative estimation of the pancreatic islet tissue in diabetic subjects. Diabetes 1955, 4:367-376.
100. Larsen M.O., Rolin B., Wilken M., Carr R.D., Gotfredsen C.F. Measurements of insulin secretory capacity and glucose tolerance to predict pancreatic beta-cell mass in vivo in the nicotinamide/streptozotocin Gottingen minipig, a model of moderate insulin deficiency and diabetes. Diabetes 2003, 52:118-123.
101. Montanya E., Nacher V., Biarnes M., Soler J. Linear correlation between beta-cell mass and body weight throughout the lifespan in Lewis rats: role of beta-cell hyperplasia and hypertrophy. Diabetes 2000, 49:1341-1346.
102. Bock T., Pakkenberg B., Buschard K. Genetic background determines the size and structure of the endocrine pancreas. Diabetes 2005, 54:133-137.
103. Rankin M.M., Kushner J.A. Adaptive beta-cell proliferation is severely restricted with advanced age. Diabetes 2009, 58:1365-1372.
104. Society for Laboratory Animal Science (GV-Solas) TVfTT. Empfehlung zur Blutentnahme bei Versuchstieren, insbesondere kleinen Versuchstieren. 2009.
105. Larsen M.O., Rolin B., Wilken M., Carr R.D., Svendsen O., Bollen P. Parameters of glucose and lipid metabolism in the male Gottingen minipig: influence of age, body weight, and breeding family. Comp Med 2001, 51:436-442.
106. Thomas L. Labor und Diagnose: Indikation und Bewertung von Laborbefunden für die medizinische Diagnostik 2012, TH-Books, Frankfurt am Main, Germany. Eight edition.
107. Kraft W., Duerr U.M. Klinische Labordiagnostik in der Tiermedizin 1999, Schattauer, Stuttgart, Germany. Fifth edition.
108. Laber-Laird K., Swindle M., Flecknell P. Handbook of rodent and rabbit medicine 1996, Pergamon Verlag, Ibbenbüren, Germany.
109. Marigliano M., Casu A., Bertera S., Trucco M., Bottino R. Hemoglobin A1C percentage in nonhuman primates: a useful tool to monitor diabetes before and after porcine pancreatic islet xenotransplantation. J Transplant 2011, 2011:965605.
110. Pyndt Jorgensen B., Hansen J.T., Krych L., Larsen C., Klein A.B., Nielsen D.S., et al. A possible link between food and mood: dietary impact on gut microbiota and behavior in BALB/c mice. PLoS One 2014, 9:e103398.
111. Shen K.P., Hao C.L., Yen H.W., Chen C.Y., Wu B.N., Lin H.L. Pre-germinated brown rice prevents high-fat diet induced hyperglycemia through elevated insulin secretion and glucose metabolism pathway in C57BL/6J strain mice. J Clin Biochem Nutr 2015, 56:28-34.
112. Williams-Fritze M.J., Smith P.C., Zelterman D., Scholz J.A. Fructosamine reference ranges in rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci 2011, 50:462-465.
113. Shlomo Melmed M., Polonsky K.S., Larsen P.R., Kronenberg H.M. Williams Textbook of Endocrinology 2011, Elsevier Saunders, Philadelphia. Twelfth edition.
114. Gardner D.G., Shoback D. Greenspan's Basic and Clinical Endocrinology 2011, McGraw-Hill Education/Medical, New York City, USA. Ninth edition.
115. Graham M.L., Bellin M.D., Papas K.K., Hering B.J., Schuurman H.J. Species incompatibilities in the pig-to-macaque islet xenotransplant model affect transplant outcome: a comparison with allotransplantation. Xenotransplantation 2011, 18:328-342.
116. Innes J.T., Carey L.C. Normal pancreatic dimensions in the adult human. Am J Surg 1994, 167:261-263.
117. Jay T.R., Heald K.A., Carless N.J., Topham D.E., Downing R. The distribution of porcine pancreatic beta-cells at ages 5, 12 and 24 weeks. Xenotransplantation 1999, 6:131-140.
118. El-Gohary Y., Sims-Lucas S., Lath N., Tulachan S., Guo P., Xiao X., et al. Three-dimensional analysis of the islet vasculature. Anat Rec (Hoboken) 2012, 295:1473-1481.
119. Wang X., Misawa R., Zielinski M.C., Cowen P., Jo J., Periwal V., 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:e67454.
120. Albl B, Haesner S, Braun-Reichhart C, Streckel E, Renner S, Seeliger F, et al. Tissue sampling guides for porcine biomedical models. Toxicol Pathol 44, 414-420.
121. Brandhorst D., Brandhorst H., Hering B.J., Federlin K., Bretzel R.G. Islet isolation from the pancreas of large mammals and humans: 10 years of experience. Exp Clin Endocrinol Diabetes 1995, 103 Suppl 2:3-14.
122. Kim A., Miller K., Jo J., Kilimnik G., Wojcik P., Hara M. Islet architecture: a comparative study. Islets 2009, 1:129-136.
123. Jorns A., Barklage E., Grube D. Heterogeneities of the islets in the rabbit pancreas and the problem of "paracrine" regulation of islet cells. Anat Embryol 1988, 178:297-307.
124. Hoang D.T., Matsunari H., Nagaya M., Nagashima H., Millis J.M., Witkowski P., et al. A conserved rule for pancreatic islet organization. PLoS One 2014, 9:e110384.
125. Bosco D., Armanet M., Morel P., Niclauss N., Sgroi A., Muller Y.D., et al. Unique arrangement of alpha- and beta-cells in human islets of Langerhans. Diabetes 2010, 59:1202-1210.
126. Buxbaum J.N. Animal models of human amyloidoses: are transgenic mice worth the time and trouble?. FEBS Lett 2009, 583:2663-2673.
127. Rahier J., Guiot Y., Goebbels R.M., Sempoux C., Henquin J.C. Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab 2008, 10 Suppl 4:32-42.
128. Bock T., Kyhnel A., Pakkenberg B., Buschard K. The postnatal growth of the beta-cell mass in pigs. J Endocrinol 2003, 179:245-252.
129. Saisho Y., Manesso E., Butler A.E., Galasso R., Kavanagh K., Flynn M., et al. Ongoing beta-cell turnover in adult nonhuman primates is not adaptively increased in streptozotocin-induced diabetes. Diabetes 2011, 60:848-856.
130. Larsen M.O., Wilken M., Gotfredsen C.F., Carr R.D., Svendsen O., Rolin B. Mild streptozotocin diabetes in the Gottingen minipig. A novel model of moderate insulin deficiency and diabetes. Am J Physiol Endocrinol Metab 2002, 282:E1342-E1351.
131. Bonner-Weir S. Regulation of pancreatic beta-cell mass in vivo. Recent Prog Horm Res 1994, 49:91-104.
132. Jo J., Kilimnik G., Kim A., Guo C., Periwal V., Hara M. Formation of pancreatic islets involves coordinated expansion of small islets and fission of large interconnected islet-like structures. Biophys J 2011, 101:565-574.
133. Bonner-Weir S., Li W.C., Ouziel-Yahalom L., Guo L., Weir G.C., Sharma A. Beta-cell growth and regeneration: replication is only part of the story. Diabetes 2010, 59:2340-2348.
134. Tschen S.I., Dhawan S., Gurlo T., Bhushan A. Age-dependent decline in beta-cell proliferation restricts the capacity of beta-cell regeneration in mice. Diabetes 2009, 58:1312-1320.
135. Meier J.J., Butler A.E., Saisho Y., Monchamp T., Galasso R., Bhushan A., et al. Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 2008, 57:1584-1594.
136. Butler A.E., Janson J., Soeller W.C., Butler P.C. Increased beta-cell apoptosis prevents adaptive increase in beta-cell mass in mouse model of type 2 diabetes: evidence for role of islet amyloid formation rather than direct action of amyloid. Diabetes 2003, 52:2304-2314.
137. Sullivan B.A., Hollister-Lock J., Bonner-Weir S., Weir G.C. Reduced Ki67 staining in the postmortem state calls into question past conclusions about the lack of turnover of adult human beta-cells. Diabetes 2015, 64:1698-1702.
138. Larsen M.O., Rolin B., Raun K., Bjerre Knudsen L., Gotfredsen C.F., Bock T. Evaluation of beta-cell mass and function in the Gottingen minipig. Diabetes Obes Metab 2007, 9 Suppl 2:170-179.
139. Guardado-Mendoza R., Jimenez-Ceja L., Majluf-Cruz A., Kamath S., Fiorentino T.V., Casiraghi F., et al. Impact of obesity severity and duration on pancreatic beta- and alpha-cell dynamics in normoglycemic non-human primates. Int J Obes 2013, 37:1071-1078.
140. Tibaldi J.M. Incorporating incretin-based therapies into clinical practice for patients with type 2 diabetes. Adv Ther 2014, 31:289-317.
141. Sandel A.A. Brief communication: hair density and body mass in mammals and the evolution of human hairlessness. Am J Phys Anthropol 2013, 152:145-150.
142. Debeer S., Le Luduec J.B., Kaiserlian D., Laurent P., Nicolas J.F., Dubois B., et al. Comparative histology and immunohistochemistry of porcine versus human skin. Eur J Dermatol 2013, 23:456-466.
143. Harms M., Seale P. Brown and beige fat: development, function and therapeutic potential. Nat Med 2013, 19:1252-1263.
144. Lidell M.E., Betz M.J., Dahlqvist Leinhard O., Heglind M., Elander L., Slawik M., et al. Evidence for two types of brown adipose tissue in humans. Nat Med 2013, 19:631-634.
145. Cypess A.M., Lehman S., Williams G., Tal I., Rodman D., Goldfine A.B., et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med 2009, 360:1509-1517.
146. Wu J., Bostrom P., Sparks L.M., Ye L., Choi J.H., Giang A.H., et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012, 150:366-376.
147. Meier J.J., Nauck M.A. Incretin-based therapies: where will we be 50 years from now?. Diabetologia 2015, 58:1745-1750.
148. Kang M.J., Kim H.G., Kim J.S., Oh do G., Um Y.J., Seo C.S., et al. The effect of gut microbiota on drug metabolism. Expert Opin Drug Metab Toxicol 2013, 9:1295-1308.
149. Horn C.C., Kimball B.A., Wang H., Kaus J., Dienel S., Nagy A., et al. Why can't rodents vomit? A comparative behavioral, anatomical, and physiological study. PLoS One 2013, 8:e60537.
150. Dalgaard L. Comparison of minipig, dog, monkey and human drug metabolism and disposition. J Pharmacol Toxicol Methods 2015, 74:80-92.
151. Helke K.L., Swindle M.M. Animal models of toxicology testing: the role of pigs. Expert Opin Drug Metab Toxicol 2013, 9:127-139.
152. Davies B., Morris T. Physiological parameters in laboratory animals and humans. Pharm Res 1993, 10:1093-1095.
153. Vaughan K.L., Szarowicz M.D., Herbert R.L., Mattison J.A. Comparison of anesthesia protocols for intravenous glucose tolerance testing in rhesus monkeys. J Med Primatol 2014, 43:162-168.
154. Tanaka K., Kawano T., Tomino T., Kawano H., Okada T., Oshita S., et al. Mechanisms of impaired glucose tolerance and insulin secretion during isoflurane anesthesia. Anesthesiology 2009, 111:1044-1051.
155. Ramsay T.G., White M.E. Insulin regulation of leptin expression in streptozotocin diabetic pigs. J Anim Sci 2000, 78:1497-1503.
156. Higgins P.J., Garlick R.L., Bunn H.F. Glycosylated hemoglobin in human and animal red cells. Role of glucose permeability. Diabetes 1982, 31:743-748.
157. Bollen P.J., Madsen L.W., Meyer O., Ritskes-Hoitinga J. Growth differences of male and female Gottingen minipigs during ad libitum feeding: a pilot study. Lab Anim 2005, 39:80-93.
158. Etherton T.D., Kris-Etherton P.M. Characterization of plasma lipoproteins in swine with different propensities for obesity. Lipids 1980, 15:823-829.
159. Burgos-Paz W., Souza C.A., Megens H.J., Ramayo-Caldas Y., Melo M., Lemús-Flores C., Caal E., Soto H.W., Martínez R., Alvarez L.A., Aguirre L., Iñiguez V., Revidatti M.A., Martínez-López O.R., Llambi S., Esteve-Codina A., Rodríguez M.C., Crooijmans R.P., Paiva S.R., Schook L.B., Groenen M.A., Pérez-Enciso M. Porcine colonization of the Americas: a 60k SNP story. Heredity (Edinb) 2013, 110:321-330.
160. Munoz G., Ovilo C., Silio L., Tomas A., Noguera J.L., Rodriguez M.C. Single- and joint-population analyses of two experimental pig crosses to confirm quantitative trait loci on Sus scrofa chromosome 6 and leptin receptor effects on fatness and growth traits. J Anim Sci 2009, 87:459-468.
161. Torres-Rovira L., Gonzalez-Anover P., Astiz S., Caro A., Lopez-Bote C., Ovilo C., et al. Effect of an obesogenic diet during the juvenile period on growth pattern, fatness and metabolic, cardiovascular and reproductive features of Swine with obesity/leptin resistance. Endocr Metab Immune Disord Drug Targets 2013, 13:143-151.
162. Cirera S., Jensen M.S., Elbrond V.S., Moesgaard S.G., Christoffersen B.O., Kadarmideen H.N., et al. Expression studies of six human obesity-related genes in seven tissues from divergent pig breeds. Anim Genet 2014, 45:59-66.
163. Dyson M.C., Alloosh M., Vuchetich J.P., Mokelke E.A., Sturek M. Components of metabolic syndrome and coronary artery disease in female Ossabaw swine fed excess atherogenic diet. Comp Med 2006, 56:35-45.
164. Christoffersen B.O., Grand N., Golozoubova V., Svendsen O., Raun K. Gender-associated differences in metabolic syndrome-related parameters in Gottingen minipigs. Comp Med 2007, 57:493-504.
165. Kanter R., Caballero B. Global gender disparities in obesity: a review. Adv Nutr 2012, 3:491-498.
166. Christoffersen B.O., Gade L.P., Golozoubova V., Svendsen O., Raun K. Influence of castration-induced testosterone and estradiol deficiency on obesity and glucose metabolism in male Gottingen minipigs. Steroids 2010, 75:676-684.
167. Christoffersen B., Golozoubova V., Pacini G., Svendsen O., Raun K. The young Gottingen minipig as a model of childhood and adolescent obesity: influence of diet and gender. Obesity 2013, 21:149-158.
168. Dixon J.L., Stoops J.D., Parker J.L., Laughlin M.H., Weisman G.A., Sturek M. Dyslipidemia and vascular dysfunction in diabetic pigs fed an atherogenic diet. Arterioscler Thromb Vasc Biol 1999, 19:2981-2992.
169. Gerrity R.G., Natarajan R., Nadler J.L., Kimsey T. Diabetes-induced accelerated atherosclerosis in swine. Diabetes 2001, 50:1654-1665.
170. Johansen T., Hansen H.S., Richelsen B., Malmlof R. The obese Gottingen minipig as a model of the metabolic syndrome: dietary effects on obesity, insulin sensitivity, and growth hormone profile. Comp Med 2001, 51:150-155.
171. Pawar A.S., Zhu X.Y., Eirin A., Tang H., Jordan K.L., Woollard J.R., et al. Adipose tissue remodeling in a novel domestic porcine model of diet-induced obesity. Obesity 2015, 23:399-407.
172. te Pas M.F., Koopmans S.J., Kruijt L., Calus M.P., Smits M.A. Plasma proteome profiles associated with diet-induced metabolic syndrome and the early onset of metabolic syndrome in a pig model. PLoS One 2013, 8:e73087.
173. van den Heuvel M., Sorop O., Koopmans S.J., Dekker R., de Vries R., van Beusekom H.M., et al. Coronary microvascular dysfunction in a porcine model of early atherosclerosis and diabetes. Am J Physiol Heart Circ Physiol 2012, 302:H85-H94.
174. Xi S., Yin W., Wang Z., Kusunoki M., Lian X., Koike T., et al. A minipig model of high-fat/high-sucrose diet-induced diabetes and atherosclerosis. Int J Exp Pathol 2004, 85:223-231.
175. Torres-Rovira L., Astiz S., Caro A., Lopez-Bote C., Ovilo C., Pallares P., et al. Diet-induced swine model with obesity/leptin resistance for the study of metabolic syndrome and type 2 diabetes. ScientificWorldJournal 2012, 2012:510149.
176. Boullion R.D., Mokelke E.A., Wamhoff B.R., Otis C.R., Wenzel J., Dixon J.L., et al. Porcine model of diabetic dyslipidemia: insulin and feed algorithms for mimicking diabetes mellitus in humans. Comp Med 2003, 53:42-52.
177. Mozaffarian D., Katan M.B., Ascherio A., Stampfer M.J., Willett W.C. Trans fatty acids and cardiovascular disease. N Engl J Med 2006, 354:1601-1613.
178. Chiu S., Sievenpiper J.L., de Souza R.J., Cozma A.I., Mirrahimi A., Carleton A.J., et al. Effect of fructose on markers of non-alcoholic fatty liver disease (NAFLD): a systematic review and meta-analysis of controlled feeding trials. Eur J Clin Nutr 2014, 68:416-423.
179. Ionut V., Liu H., Mooradian V., Castro A.V., Kabir M., Stefanovski D., et al. Novel canine models of obese prediabetes and mild type 2 diabetes. Am J Physiol Endocrinol Metab 2010, 298:E38-E48.
180. Junod A., Lambert A.E., Stauffacher W., Renold A.E. Diabetogenic action of streptozotocin: relationship of dose to metabolic response. J Clin Invest 1969, 48:2129-2139.
181. Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia 2008, 51:216-226.
182. Rerup C.C. Drugs producing diabetes through damage of the insulin secreting cells. Pharmacol Rev 1970, 22:485-518.
183. Lauder I., Abascal J., Cartwright R.A., Farndon J.R., Johnston I.D. Liver tumours following streptozotocin administration in rats and the effects of pancreatic islet cell transplantation. Carcinogenesis 1981, 2:799-803.
184. Robbiano L., Mereto E., Corbu C., Brambilla G. DNA damage induced by seven N-nitroso compounds in primary cultures of human and rat kidney cells. Mutat Res 1996, 368:41-47.
185. Elsner M., Tiedge M., Lenzen S. Mechanism underlying resistance of human pancreatic beta cells against toxicity of streptozotocin and alloxan. Diabetologia 2003, 46:1713-1714.
186. Mohanasundaram D., Drogemuller C., Brealey J., Jessup C.F., Milner C., Murgia C., et al. Ultrastructural analysis, zinc transporters, glucose transporters and hormones expression in New world primate (Callithrix jacchus) and human pancreatic islets. Gen Comp Endocrinol 2011, 174:71-79.
187. Tarkia M., Saraste A., Stark C., Vahasilta T., Savunen T., Strandberg M., et al. [18F]FDG accumulation in early coronary atherosclerotic lesions in pigs. PLoS One 2015, 10:e0131332.
188. Gabel H., Bitter-Suermann H., Henriksson C., Save-Soderbergh J., Lundholm K., Brynger H. Streptozotocin diabetes in juvenile pigs. Evaluation of an experimental model. Horm Metab Res 1985, 17:275-280.
189. Strauss A., Moskalenko V., Tiurbe C., Chodnevskaja I., Timm S., Wiegering V.A., et al. Goettingen minipigs (GMP): comparison of two different models for inducing diabetes. Diabetol Metab Syndr 2012, 4:7.
190. Fonouni H., Tahmasbi Rad M., Esmaeilzadeh M., Golriz M., Majlesara A., Mehrabi A. A simplified technique of pancreas transplantation in a porcine model. Eur Surg Res 2015, 54:24-33.
191. Lohr M., Lubbersmeyer J., Otremba B., Klapdor R., Grossner D., Kloppel G. Increase in B-cells in the pancreatic remnant after partial pancreatectomy in pigs. An immunocytochemical and functional study. Virchows Arch B Cell Pathol Incl Mol Pathol 1989, 56:277-286.
192. McCulloch D.K., Koerker D.J., Kahn S.E., Bonner-Weir S., Palmer J.P. Correlations of in vivo beta-cell function tests with beta-cell mass and pancreatic insulin content in streptozocin-administered baboons. Diabetes 1991, 40:673-679.
193. Liu M., Sun J., Cui J., Chen W., Guo H., Barbetti F., et al. INS-gene mutations: from genetics and beta cell biology to clinical disease. Mol Aspects Med 2015, 42:3-18.
194. Hetz C., Chevet E., Harding H.P. Targeting the unfolded protein response in disease. Nat Rev Drug Discov 2013, 12:703-719.
195. Hodish I., Liu M., Rajpal G., Larkin D., Holz R.W., Adams A., et al. Misfolded proinsulin affects bystander proinsulin in neonatal diabetes. J Biol Chem 2010, 285:685-694.
196. Yoshioka M., Kayo T., Ikeda T., Koizumi A. A novel locus, Mody4, distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6 (Akita) mutant mice. Diabetes 1997, 46:887-894.
197. Iacovacci V., Ricotti L., Menciassi A., Dario P. The bioartificial pancreas (BAP): biological, chemical and engineering challenges. Biochem Pharmacol 2015, 100:12-27.
198. Domingueti C.P., Dusse L.M., Carvalho M.D., de Sousa L.P., Gomes K.B., Fernandes A.P. Diabetes mellitus: the linkage between oxidative stress, inflammation, hypercoagulability and vascular complications. J Diabetes Complications 2016, 30:12-27.
199. Abbott A. Inside the first pig biobank. Nature 2015, 519:397-398.
200. Campbell J.E., Drucker D.J. Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab 2013, 17:819-837.
201. Nauck M.A., Heimesaat M.M., Orskov C., Holst J.J., Ebert R., Creutzfeldt W. Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J Clin Invest 1993, 91:301-307.
202. Renner S., Blutke A., Streckel E., Wanke R., Wolf E. Incretin actions and consequences of incretin-based therapies: lessons from complementary animal models. J Pathol 2016, 238:345-358.
203. Symonds M.E., Sebert S.P., Hyatt M.A., Budge H. Nutritional programming of the metabolic syndrome. Nat Rev Endocrinol 2009, 5:604-610.
204. Reynolds W.A., Chez R.A., Bhuyan B.K., Neil G.L. Placental transfer of streptozotocin in the rhesus monkey. Diabetes 1974, 23:777-782.