Transgenic expression of the human growth hormone minigene promotes pancreatic β-cell proliferation

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 309, Issue 7, 2015, Pages R788-R794

  Baan, Mieke ^a   Kibbe, Carly R ^a   Bushkofsky, Justin R ^a   Harris, Ted W ^a   Sherman, Dawn S ^a   Davis, Dawn Belt ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

Author keywords

FoxM1; Human growth hormone; Proliferation; Transgene expression; cell

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR; GLUCOSE TRANSPORTER 2; HUMAN GROWTH HORMONE; INSULIN; MESSENGER RNA; PROLACTIN RECEPTOR; PROTEIN SH2; TRANSCRIPTION FACTOR FORKHEAD BOX M1; TRYPTOPHAN HYDROXYLASE; TRYPTOPHAN HYDROXYLASE 2; UNCLASSIFIED DRUG; ANTIMETABOLITE; BROXURIDINE; FOXM1 PROTEIN, MOUSE; GLUCOSE; GLUCOSE BLOOD LEVEL; SLC2A2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; INSULIN RELEASE; INSULIN SENSITIVITY; INTRON; MALE; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STOP CODON; UPREGULATION; ANIMAL; BIOSYNTHESIS; GENETICS; HUMAN; METABOLISM; PHENOTYPE; PHYSIOLOGY; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; ANTIMETABOLITES; BLOOD GLUCOSE; BROMODEOXYURIDINE; CELL PROLIFERATION; FORKHEAD TRANSCRIPTION FACTORS; GLUCOSE; GLUCOSE TRANSPORTER TYPE 2; HUMAN GROWTH HORMONE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, TRANSGENIC; PHENOTYPE; RNA, MESSENGER; TRANSGENES;

EID: 84943183391     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00244.2015     Document Type: Article

References (39)

1. Albers KM, Davis FE, Perrone TN, Lee EY, Liu Y, Vore M. Expression of an epidermal keratin protein in liver of transgenic mice causes structural and functional abnormalities. J Cell Biol 128: 157-169, 1995.
2. Brinster RL, Allen JM, Behringer RR, Gelinas RE, Palmiter RD. Introns increase transcriptional efficiency in transgenic mice. Proc Natl Acad Sci USA 85: 836-840, 1988.
3. Brouwers B, de Faudeur G, Osipovich AB, Goyvaerts L, Lemaire K, Boesmans L, Cauwelier EJ, Granvik M, Pruniau VP, Van Lommel L, Van Schoors J, Stancill JS, Smolders I, Goffin V, Binart N, in't Veld P, Declercq J, Magnuson MA, Creemers JW, Schuit F, Schraenen A. Impaired islet function in commonly used transgenic mouse lines due to human growth hormone minigene expression. Cell Metab 20: 979-990, 2014.
4. Clee SM, Nadler ST, Attie AD. Genetic and genomic studies of the BTBR ob/ob mouse model of type 2 diabetes. Am J Ther 12: 491-498, 2005.
5. Clee SM, Yandell BS, Schueler KM, Rabaglia ME, Richards OC, Raines SM, Kabara EA, Klass DM, Mui ET, Stapleton DS, Gray-Keller MP, Young MB, Stoehr JP, Lan H, Boronenkov I, Raess PW, Flowers MT, Attie AD. Positional cloning of Sorcs1, a type 2 diabetes quantitative trait locus. Nat Genet 38: 688-693, 2006.
6. Davis DB, Lavine JA, Suhonen JI, Krautkramer KA, Rabaglia ME, Sperger JM, Fernandez LA, Yandell BS, Keller MP, Wang IM, Schadt EE, Attie AD. FoxM1 is up-regulated by obesity and stimulates β-cell proliferation. Mol Endocrinol 24: 1822-1834, 2010.
7. Garcia-Ocana A, Takane KK, Syed MA, Philbrick WM, Vasavada RC, Stewart AF. Hepatocyte growth factor overexpression in the islet of transgenic mice increases beta cell proliferation, enhances islet mass, and induces mild hypoglycemia. J Biol Chem 275: 1226-1232, 2000.
8. Hara M, Dizon RF, Glick BS, Lee CS, Kaestner KH, Piston DW, Bindokas VP. Imaging pancreatic beta-cells in the intact pancreas. Am J Physiol Endocrinol Metab 290: E1041-E1047, 2006.
9. Hara M, Wang X, Kawamura T, Bindokas VP, Dizon RF, Alcoser SY, Magnuson MA, Bell GI. Transgenic mice with green fluorescent proteinlabeled pancreatic beta-cells. Am J Physiol Endocrinol Metab 284: E177-E183, 2003.
10. Hodish I, Liu M, Rajpal G, Larkin D, Holz RW, Adams A, Liu L, Arvan P. Misfolded proinsulin affects bystander proinsulin in neonatal diabetes. J Biol Chem 285: 685-694, 2010.
11. Hosokawa YA, Leahy JL. Parallel reduction of pancreas insulin content and insulin secretion in 48-h tolbutamide-infused normoglycemic rats. Diabetes 46: 808-813, 1997.
12. Huang X, Zhao YY. Transgenic expression of FoxM1 promotes endothelial repair following lung injury induced by polymicrobial sepsis in mice. PloS One 7: e50094, 2012.
13. Kalinichenko VV, Gusarova GA, Tan Y, Wang IC, Major ML, Wang X, Yoder HM, Costa RH. Ubiquitous expression of the forkhead box M1B transgene accelerates proliferation of distinct pulmonary cell types following lung injury. J Biol Chem 278: 37, 888-37, 894, 2003.
14. Keller MP, Choi Y, Wang P, Davis DB, Rabaglia ME, Oler AT, Stapleton DS, Argmann C, Schueler KL, Edwards S, Steinberg HA, Chaibub Neto E, Kleinhanz R, Turner S, Hellerstein MK, Schadt EE, Yandell BS, Kendziorski C, Attie AD. A gene expression network model of type 2 diabetes links cell cycle regulation in islets with diabetes susceptibility. Genome Res 18: 706-716, 2008.
15. Kong J, Crissey MA, Funakoshi S, Kreindler JL, Lynch JP. Ectopic Cdx2 expression in murine esophagus models an intermediate stage in the emergence of Barrett's esophagus. PloS One 6: e18280, 2011.
16. Lee JY, Ristow M, Lin X, White MF, Magnuson MA, Hennighausen L. RIP-Cre revisited, evidence for impairments of pancreatic beta-cell function. J Biol Chem 281: 2649-2653, 2006.
17. Lin X, Jia J, Du T, Li W, Wang X, Wei J, Lin X, Zeng H, Yao L, Chen X, Zhuang J, Weng J, Liu Y, Lin J, Wu Q, Wang W, Yao K, Xu K, Xiao D. Overexpression of miR-155 in the liver of transgenic mice alters the expression profiling of hepatic genes associated with lipid metabolism. PloS One 10: e0118417, 2015.
18. Linnemann AK, Neuman JC, Battiola TJ, Wisinski JA, Kimple ME, Davis DB. Glucagon-like peptide-1 regulates cholecystokinin production in beta-cells to protect from apoptosis. Mol Endocrinol me20151030, 2015.
19. Neuman JC, Truchan NA, Joseph JW, Kimple ME. A method for mouse pancreatic islet isolation and intracellular cAMP determination. J Vis Exp JoVE e50374, 2014.
20. Palmiter RD, Norstedt G, Gelinas RE, Hammer RE, Brinster RL. Metallothionein-human GH fusion genes stimulate growth of mice. Science 222: 809-814, 1983.
21. Palmiter RD, Sandgren EP, Avarbock MR, Allen DD, Brinster RL. Heterologous introns can enhance expression of transgenes in mice. Proc Natl Acad Sci USA 88: 478-482, 1991.
22. Park SY, Wang X, Chen Z, Powers AC, Magnuson MA, Head WS, Piston DW, Bell GI. Optical imaging of pancreatic beta cells in living mice expressing a mouse insulin I promoter-firefly luciferase transgene. Genesis 43: 80-86, 2005.
23. Postic C, Shiota M, Niswender KD, Jetton TL, Chen Y, Moates JM, Shelton KD, Lindner J, Cherrington AD, Magnuson MA. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J Biol Chem 274: 305-315, 1999.
24. Qvartskhava N, Lang PA, Gorg B, Pozdeev VI, Ortiz MP, Lang KS, Bidmon HJ, Lang E, Leibrock CB, Herebian D, Bode JG, Lang F, Haussinger D. Hyperammonemia in gene-targeted mice lacking functional hepatic glutamine synthetase. Proc Natl Acad Sci USA 112: 5521-5526, 2015.
25. Rachidi S, Sun S, Wu BX, Jones E, Drake RR, Ogretmen B, Cowart LA, Clarke CJ, Hannun YA, Chiosis G, Liu B, Li Z. Endoplasmic reticulum heat shock protein gp96 maintains liver homeostasis and promotes hepatocellular carcinogenesis. J Hepatol 62: 879-888, 2015.
26. Sandgren EP, Luetteke NC, Palmiter RD, Brinster RL, Lee DC. Overexpression of TGF-alpha in transgenic mice: induction of epithelial hyperplasia, pancreatic metaplasia, and carcinoma of the breast. Cell 61: 1121-1135, 1990.
27. Scheving LA, Zhang X, Stevenson MC, Threadgill DW, Russell WE. Loss of hepatocyte EGFR has no effect alone but exacerbates carbon tetrachloride-induced liver injury and impairs regeneration in hepatocyte Met-deficient mice. Am J Physiol Gastrointest Liver Physiol 308: G364-G377, 2015.
28. Stoehr JP, Nadler ST, Schueler KL, Rabaglia ME, Yandell BS, Metz SA, Attie AD. Genetic obesity unmasks nonlinear interactions between murine type 2 diabetes susceptibility loci. Diabetes 49: 1946-1954, 2000.
29. Takamoto I, Kubota N, Nakaya K, Kumagai K, Hashimoto S, Kubota T, Inoue M, Kajiwara E, Katsuyama H, Obata A, Sakurai Y, Iwamoto M, Kitamura T, Ueki K, Kadowaki T. TCF7L2 in mouse pancreatic beta cells plays a crucial role in glucose homeostasis by regulating beta cell mass. Diabetologia 57: 542-553, 2014.
30. Tamarina NA, Roe MW, Philipson L. Characterization of mice expressing Ins1 gene promoter driven CreERT recombinase for conditional gene deletion in pancreatic beta-cells. Islets 6: e27685, 2014.
31. Vasavada RC, Cavaliere C, D'Ercole AJ, Dann P, Burtis WJ, Madlener AL, Zawalich K, Zawalich W, Philbrick W, Stewart AF. Overexpression of parathyroid hormone-related protein in the pancreatic islets of transgenic mice causes islet hyperplasia, hyperinsulinemia, and hypoglycemia. J Biol Chem 271: 1200-1208, 1996.
32. Vasavada RC, Garcia-Ocana A, Zawalich WS, Sorenson RL, Dann P, Syed M, Ogren L, Talamantes F, Stewart AF. Targeted expression of placental lactogen in the beta cells of transgenic mice results in beta cell proliferation, islet mass augmentation, and hypoglycemia. J Biol Chem 275: 15, 399-15, 406, 2000.
33. Vassar R, Fuchs E. Transgenic mice provide new insights into the role of TGF-α during epidermal development and differentiation. Genes Dev 5: 714-727, 1991.
34. Wang X, Quail E, Hung NJ, Tan Y, Ye H, Costa RH. Increased levels of forkhead box M1B transcription factor in transgenic mouse hepatocytes prevent age-related proliferation defects in regenerating liver. Proc Natl Acad Sci USA 98: 11, 468-11, 473, 2001.
35. Wierstra I. The transcription factor FOXM1 (Forkhead box M1): proliferationspecific expression, transcription factor function, target genes, mouse models, and normal biological roles. Adv Cancer Res 118: 97-398, 2013.
36. Wysolmerski JJ, Broadus AE, Zhou J, Fuchs E, Milstone LM, Philbrick WM. Overexpression of parathyroid hormone-related protein in the skin of transgenic mice interferes with hair follicle development. Proc Natl Acad Sci USA 91: 1133-1137, 1994.
37. Wysolmerski JJ, McCaughern-Carucci JF, Daifotis AG, Broadus AE, Philbrick WM. Overexpression of parathyroid hormone-related protein or parathyroid hormone in transgenic mice impairs branching morphogenesis during mammary gland development. Development 121: 3539-3547, 1995.
38. Ye H, Holterman AX, Yoo KW, Franks RR, Costa RH. Premature expression of the winged helix transcription factor HFH-11B in regenerating mouse liver accelerates hepatocyte entry into S phase. Mol Cell Biol 19: 8570-8580, 1999.
39. Zhang X, Degenstein L, Cao Y, Stein J, Osei K, Wang J. beta-Cells with relative low HIMP1 overexpression levels in a transgenic mouse line enhance basal insulin production and hypoxia/hypoglycemia tolerance. PloS One 7: e34126, 2012.