Prolonged Cre expression driven by the α-myosin heavy chain promoter can be cardiotoxic

Journal of Molecular and Cellular Cardiology

Volumn 86, Issue , 2015, Pages 54-61

  Pugach, Emily K ^a   Richmond, Phillip A ^a   Azofeifa, Joseph G ^b   Dowell, Robin D ^a   Leinwand, Leslie A ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UCB 450   (United States)

Author keywords

Cardiotoxicity; Cre recombinase; DNA damage; LoxP site; Transgenic mice

Indexed keywords

CRE RECOMBINASE; MYOSIN HEAVY CHAIN ALPHA; INTEGRASE; MYH6 PROTEIN, MOUSE; MYOSIN HEAVY CHAIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIOPHAGE; BIOINFORMATICS; CARDIOTOXICITY; CONTROLLED STUDY; DNA DAMAGE; DNA EDITING; FEMALE; FIBROSIS; GENE DISRUPTION; GENE EXPRESSION; GENOME; GENOTYPE; HEART FUNCTION; HEART MUSCLE CELL; IN VIVO STUDY; INFLAMMATION; KNOCKOUT MOUSE; LOXP SITE; MALE; MOUSE; MUSCLE FUNCTION; NONHUMAN; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SEX DIFFERENCE; ANIMAL; BIOSYNTHESIS; CARDIAC MUSCLE CELL; GENETICS; HUMAN; METABOLISM; PATHOLOGY;

MUS; MUS MUSCULUS;

ANIMALS; CARDIOTOXICITY; DNA DAMAGE; GENOTYPE; HUMANS; INTEGRASES; MICE; MICE, KNOCKOUT; MYOCYTES, CARDIAC; MYOSIN HEAVY CHAINS; PROMOTER REGIONS, GENETIC;

EID: 84937400078     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.06.019     Document Type: Article

References (48)

1. Agah R., Frenkel P.A., French B.A., Michael L.H., Overbeek P.A., Schneider M.D. Gene Recombination in Postmitotic Cells. Targeted Expression of Cre Recombinase Provokes Cardiac-Restricted, Site-Specific Rearrangement in Adult Ventricular Muscle In Vivo 1997, 169-179.
2. Branda C.S., Dymecki S.M. Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 2004, 6:7-28.
3. Subramaniam A., Jones W.K., Gulick J., Wert S., Neumann J., Robbins J. Tissue-specific regulation of the alpha-myosin heavy chain gene promoter in transgenic mice. J. Biol. Chem. 1991, 266:24613-24620.
4. Sternberg N., Hamilton D., Austin S., Yarmolinsky M., Hoess R. Site-specific recombination and its role in the life cycle of bacteriophage P1. Cold Spring Harb. Symp. Quant. Biol. 1981, 45:297-309.
5. Hoess R.H., Wierzbicki A., Abremski K. The role of the loxP spacer region in P1 site-specific recombination. Nucleic Acids Res. 1986, 14:2287-2300.
6. Thyagarajan B., Guimarães M.J., Groth A.C., Calos M.P. Mammalian genomes contain active recombinase recognition sites. Gene 2000, 244:47-54.
7. Ito M., Yamanouchi K., Naito K., Calos M.P., Tojo H. Site-specific integration of transgene targeting an endogenous lox-like site in early mouse embryos. J. Appl. Genet. 2011, 52:89-94.
8. Iovino N., Denti M.A., Bozzoni I., Cortese R. A loxP-containing pol II promoter for RNA interference is reversibly regulated by Cre recombinase. RNA Biol. 2005, 2:86-92.
9. Janbandhu V., Moik D., Fässler R. Cre recombinase induces DNA damage and tetraploidy in the absence of LoxP sites. Cell Cycle 2014, 13:462-470.
10. Schmidt E.E., Taylor D.S., Prigge J.R., Barnett S., Capecchi M.R. Illegitimate Cre-dependent chromosome rearrangements in transgenic mouse spermatids. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:13702-13707.
11. Harno E., Cottrell E.C., White A. Metabolic pitfalls of CNS Cre-based technology. Cell Metab. 2013, 18:21-28.
12. Huh W.J., Mysorekar I.U., Mills J.C. Inducible activation of Cre recombinase in adult mice causes gastric epithelial atrophy, metaplasia, and regenerative changes in the absence of "floxed" alleles. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G368-G380.
13. Lexow J., Poggioli T., Sarathchandra P., Santini M.P., Rosenthal N. Cardiac fibrosis in mice expressing an inducible myocardial-specific Cre driver. Dis. Model. Mech. 2013, 6:1470-1476.
14. Bersell K., Choudhury S., Mollova M., Polizzotti B.D., Ganapathy B., Walsh S., et al. Moderate and high amounts of tamoxifen in αMHC-MerCreMer mice induce a DNA damage response, leading to heart failure and death. Dis. Model. Mech. 2013, 6:1459-1469.
15. Buerger A., Rozhitskaya O., Sherwood M.C., Dorfman A.L., Bisping E., Abel E.D., et al. Dilated cardiomyopathy resulting from high-level myocardial expression of Cre-recombinase. J. Card. Fail. 2006, 12:392-398.
16. Koitabashi N., Bedja D., Zaiman A.L., Pinto Y.M., Zhang M., Gabrielson K.L., et al. Avoidance of transient cardiomyopathy in cardiomyocyte-targeted tamoxifen-induced MerCreMer gene deletion models. Circ. Res. 2009, 105:12-15.
17. Doetschman T., Azhar M. Cardiac-specific inducible and conditional gene targeting in mice. Circ. Res. 2012, 110:1498-1512.
18. Davis J., Maillet M., Miano J.M., Molkentin J.D. Lost in transgenesis: a user's guide for genetically manipulating the mouse in cardiac research. Circ. Res. 2012, 111:761-777.
19. Molkentin J.D., Robbins J. With great power comes great responsibility: using mouse genetics to study cardiac hypertrophy and failure. J. Mol. Cell. Cardiol. 2009, 46:130-136.
20. Bush E., Fielitz J., Melvin L., Martinez-Arnold M., McKinsey T.A., Plichta R., et al. A small molecular activator of cardiac hypertrophy uncovered in a chemical screen for modifiers of the calcineurin signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2870-2875.
21. Schulz K.U., Mihov S. Fast string correction with Levenshtein automata. IJDAR 2002, 5:67-85.
22. Aho A.V., Corasick M.J. Efficient string matching: an aid to bibliographic search. Commun. ACM 1975, 18:333-340.
23. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
24. Joshi M.U., Pittman H.K., Haisch C.E., Verbanac K.M. Real-time PCR to determine transgene copy number and to quantitate the biolocalization of adoptively transferred cells from EGFP-transgenic mice. Biotechniques 2008, 45:247-258.
25. Pillai M.M., Venkataraman G.M., Kosak S., Torok-Storb B. Integration site analysis in transgenic mice by thermal asymmetric interlaced (TAIL)-PCR: segregating multiple-integrant founder lines and determining zygosity. Transgenic Res. 2008, 17:749-754.
26. Liu Y.G., Whittier R.F. Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 1995, 25:674-681.
27. Luczak E.D., Leinwand L.A. Sex-based cardiac physiology. Annu. Rev. Physiol. 2009, 71:1-18.
28. Schaefer S., Taylor A.L., Lee H.R., Niggemann E.H., Levine B.D., Popma J.J., et al. Effect of increasing heart rate on left ventricular performance in patients with normal cardiac function. Am. J. Cardiol. 1988, 61:617-620.
29. Higgins C.B., Vatner S.F., Franklin D., Braunwald E. Extent of regulation of the heart's contractile state in the conscious dog by alteration in the frequency of contraction 1973, 52:1187-1194.
30. Villarreal F.J., Dillmann W.H. Cardiac hypertrophy-induced changes in mRNA levels for TGF-beta 1, fibronectin, and collagen. Am. J. Physiol. 1992, 262:H1861-H1866.
31. Konhilas J.P., Watson P.A., Maass A., Boucek D.M., Horn T., Stauffer B.L., et al. Exercise can prevent and reverse the severity of hypertrophic cardiomyopathy. Circ. Res. 2006, 98:540-548.
32. Barrick C.J., Dong A., Waikel R., Corn D., Yang F., Threadgill D.W., et al. Parent-of-origin effects on cardiac response to pressure overload in mice. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H1003-H1009.
33. Clerk A., Sugden P.H. Inflame my heart (by p38-MAPK). Circ. Res. 2006, 99:455-458.
34. Guo F., Gopaul D.N., van Duyne G.D. Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 1997, 389:40-46.
35. Matkovich S.J., Zhang Y., Van Booven D.J., Dorn G.W. Deep mRNA sequencing for in vivo functional analysis of cardiac transcriptional regulators: application to Galphaq. Circ. Res. 2010, 106:1459-1467.
36. Guan Z., Baier L.D., Morrison A.R. p38 Mitogen-activated protein kinase down-regulates nitric oxide and up-regulates prostaglandin E2 biosynthesis stimulated by interleukin-1β. J. Biol. Chem. 1997, 272:8083-8089.
37. Zechner D., Thuerauf D.J., Hanford D.S. A role for the p38 mitogen-activated protein kinase pathway in myocardial cell growth, sarcomeric organization, and cardiac-specific gene expression. J. Cell Biol. 1997, 139:115-127.
38. Molkentin J.D., Lu J.-R., Antos C.L., Markham B., Richardson J., Robbins J., et al. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 1998, 93:215-228.
39. Qiu Z., Cang Y., Goff S.P. c-Abl tyrosine kinase regulates cardiac growth and development. PNAS 2010, 107:1136-1141.
40. Schulkey C.E., Regmi S.D., Magnan R.A., Danzo M.T., Luther H., Hutchinson A.K., et al. The maternal-age-associated risk of congenital heart disease is modifiable. Nature 2015, 520:230-233.
41. Semsarian C., Healey M.J., Fatkin D., Giewat M., Duffy C., Seidman C.E., et al. A polymorphic modifier gene alters the hypertrophic response in a murine model of familial hypertrophic cardiomyopathy. J. Mol. Cell. Cardiol. 2001, 33:2055-2060.
42. Sanford L.P., Kallapur S., Ormsby I., Doetschman T. Influence of genetic background on knockout mouse phenotypes. Methods Mol. Biol. 2001, 158:217-225.
43. Bergo M.O., Lieu H.D., Gavino B.J., Ambroziak P., Otto J.C., Casey P.J., et al. On the physiological importance of endoproteolysis of CAAX proteins: heart-specific RCE1 knockout mice develop a lethal cardiomyopathy. J. Biol. Chem. 2004, 279:4729-4736.
44. Cavasin M.A., Tao Z., Menon S., Yang X.-P. Gender differences in cardiac function during early remodeling after acute myocardial infarction in mice. Life Sci. 2004, 75:2181-2192.
45. Douglas P.S., Katz S.E., Weinberg E.O., Chen M.H., Bishop S.P., Lorell B.H. Hypertrophic remodeling: gender differences in the early response to left ventricular pressure overload. J. Am. Coll. Cardiol. 1998, 32:1118-1125.
46. Abel E.D., Kaulbach H.C., Tian R., Hopkins J.C.A., Duffy J., Doetschman T., et al. Cardiac hypertrophy with preserved contractile function after selective deletion of GLUT4 from the heart 1999, 104:1703-1714.
47. Rüfer A.W., Sauer B. Non-contact positions impose site selectivity on Cre recombinase. Nucleic Acids Res. 2002, 30:2764-2771.
48. Itoh G., Tamura J., Suzuki M., Suzuki Y., Ikeda H., Koike M., et al. DNA fragmentation of human infarcted myocardial cells demonstrated by the nick end labeling method and DNA agarose gel electrophoresis. Am. J. Pathol. 1995, 146:1325-1331.