An inducible CiliaGFP mouse model for in vivo visualization and analysis of cilia in live tissue

Cilia

Volumn 2, Issue 1, 2013, Pages

  O'Connor, Amber K ^e   Malarkey, Erik B ^a   Berbari, Nicolas F ^a   Croyle, Mandy J ^a   Haycraft, Courtney J ^b   Bell, P D ^b   Hohenstein, Peter ^c   Kesterson, Robert A ^d   Yoder, Bradley K ^a  

^a UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

In vivo cilia labeling; Inducible transgene; Intravital microscopy; ROSA26 locus; Somatostatin receptor 3

Indexed keywords

COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; SOMATOSTATIN RECEPTOR 3; SOMATOSTATIN RECEPTOR 3 GREEN FLUORESCENT PROTEIN FUSION PROTEIN; UNCLASSIFIED DRUG;

ANATOMIC LANDMARK; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; BRAIN TISSUE; CELL FUNCTION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CILIARY MOTILITY; CONTROLLED STUDY; EPENDYMA CELL; EUKARYOTIC FLAGELLUM; EXPERIMENTAL MOUSE; FLUORESCENCE IMAGING; GENE; GENE LOCUS; GENE TARGETING; GLOMERULUS FILTRATION RATE; HEART BEAT; IN VIVO STUDY; KIDNEY PARENCHYMA; KIDNEY TUBULE; MOLECULAR IMAGING; MOUSE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; RETINA; ROSA26 GENE; SIGNAL TRANSDUCTION; SSTR3 GENE; TISSUE DISTRIBUTION; TRANSGENE;

EID: 84880095521     PISSN: None     EISSN: 20462530     Source Type: Journal    
DOI: 10.1186/2046-2530-2-8     Document Type: Article

References (52)

1. Oh EC, Katsanis N. Cilia in vertebrate development and disease. Development 2012, 139:443-448. 10.1242/dev.050054, 3275291, 22223675.
2. Pazour GJ, Witman GB. The vertebrate primary cilium is a sensory organelle. Curr Opin Cell Biol 2003, 15:105-110. 10.1016/S0955-0674(02)00012-1, 12517711.
3. Davenport JR, Yoder BK. An incredible decade for the primary cilium: a look at a once-forgotten organelle. Am J Physiol Renal Physiol 2005, 289:F1159-F1169. 10.1152/ajprenal.00118.2005, 16275743.
4. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK. The primary cilium as a complex signaling center. Curr Biol 2009, 19:R526-R535. 10.1016/j.cub.2009.05.025, 2814769, 19602418.
5. Hohenstein P, Slight J, Ozdemir DD, Burn SF, Berry R, Hastie ND. High-efficiency Rosa26 knock-in vector construction for Cre-regulated overexpression and RNAi. Pathogenetics 2008, 1:3. 10.1186/1755-8417-1-3, 2583990, 19014667.
6. Nagy A. Manipulating the Mouse Embryo: a Laboratory Manual 2003, 764. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 3.
7. O'Connor AK, Kesterson RA, Yoder BK. Generating conditional mutants to analyze ciliary functions: the use of Cre-lox technology to disrupt cilia in specific organs. Methods Cell Biol 2009, 93:305-330.
8. Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci U S A 1996, 93:5860-5865. 10.1073/pnas.93.12.5860, 39152, 8650183.
9. Xu AW, Kaelin CB, Takeda K, Akira S, Schwartz MW, Barsh GS. PI3K integrates the action of insulin and leptin on hypothalamic neurons. J Clin Invest 2005, 115:951-958. 1062894, 15761497.
10. Zhang H, Fujitani Y, Wright CV, Gannon M. Efficient recombination in pancreatic islets by a tamoxifen-inducible Cre-recombinase. Genesis 2005, 42:210-217. 10.1002/gene.20137, 15986486.
11. Berbari NF, Johnson AD, Lewis JS, Askwith CC, Mykytyn K. Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors. Mol Biol Cell 2008, 19:1540-1547. 10.1091/mbc.E07-09-0942, 2291422, 18256283.
12. Croyle MJ, Lehman JM, O'Connor AK, Wong SY, Malarkey EB, Iribarne D, Dowdle WE, Schoeb TR, Verney ZM, Athar M, Michaud EJ, Reiter JF, Yoder BK. Role of epidermal primary cilia in the homeostasis of skin and hair follicles. Development 2011, 138:1675-1685. 10.1242/dev.060210, 3074444, 21429982.
13. Anthony TE, Klein C, Fishell G, Heintz N. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 2004, 41:881-890. 10.1016/S0896-6273(04)00140-0, 15046721.
14. Banizs B, Pike MM, Millican CL, Ferguson WB, Komlosi P, Sheetz J, Bell PD, Schwiebert EM, Yoder BK. Dysfunctional cilia lead to altered ependyma and choroid plexus function, and result in the formation of hydrocephalus. Development 2005, 132:5329-5339. 10.1242/dev.02153, 16284123.
15. Nakamura Y, Sato KY. Role of disturbance of ependyaml ciliary function in development of hydrocephalus in rats. Childs Nerv Syst 1993, 9:65-71. 10.1007/BF00305310, 8319234.
16. Sharma N, Berbari NF, Yoder BK. Ciliary dysfunction in developmental abnormalities and diseases. Curr Top Dev Biol 2008, 85:371-427.
17. Davenport JR, Watts AJ, Roper VC, Croyle MJ, van Groen T, Wyss JM, Nagy TR, Kesterson RA, Yoder BK. Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr Biol 2007, 17:1586-1594. 10.1016/j.cub.2007.08.034, 2084209, 17825558.
18. Doherty D. Joubert syndrome: insights into brain development, cilium biology, and complex disease. Semin Pediatr Neurol 2009, 16:143-154. 10.1016/j.spen.2009.06.002, 2804071, 19778711.
19. Pazour GJ, Baker SA, Deane JA, Cole DG, Dickert BL, Rosenbaum JL, Witman GB, Besharse JC. The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J Cell Biol 2002, 157:103-113. 10.1083/jcb.200107108, 2173265, 11916979.
20. Kulaga HM, Leitch CC, Eichers ER, Badano JL, Lesemann A, Hoskins BE, Lupski JR, Beales PL, Reed RR, Katsanis N. Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat Genet 2004, 36:994-998. 10.1038/ng1418, 15322545.
21. McIntyre JC, Davis EE, Joiner A, Williams CL, Tsai IC, Jenkins PM, McEwen DP, Zhang L, Escobado J, Thomas S, Szymanska K, Johnson CA, Beales PL, Green ED, Mullikin JC, Comparative Sequencing Program NISC, Sabo A, Muzny DM, Gibbs RA, Attié-Bitach T, Yoder BK, Reed RR, Katsanis N, Martens JR. Gene therapy rescues cilia defects and restores olfactory function in a mammalian ciliopathy model. Nat Med 2012, 18:1423-1428. 10.1038/nm.2860, 3645984, 22941275.
22. Louvi A, Grove EA. Cilia in the CNS: the quiet organelle claims center stage. Neuron 2011, 69:1046-1060. 10.1016/j.neuron.2011.03.002, 3070490, 21435552.
23. Bishop GA, Berbari NF, Lewis J, Mykytyn K. Type III adenylyl cyclase localizes to primary cilia throughout the adult mouse brain. J Comp Neurol 2007, 505:562-571. 10.1002/cne.21510, 17924533.
24. Fukushima N, Furuta D, Hidaka Y, Moriyama R, Tsujiuchi T. Post-translational modifications of tubulin in the nervous system. J Neurochem 2009, 109:683-693. 10.1111/j.1471-4159.2009.06013.x, 19250341.
25. Mahjoub MR, Stearns T. Supernumerary centrosomes nucleate extra cilia and compromise primary cilium signaling. Curr Biol 2012, 22:1628-1634. 10.1016/j.cub.2012.06.057, 22840514.
26. Praetorius HA, Spring KR. Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 2001, 184:71-79. 10.1007/s00232-001-0075-4, 11687880.
27. Nauli SM, Kawanabe Y, Kaminski JJ, Pearce WJ, Ingber DE, Zhou J. Endothelial cilia are fluid shear sensors that regulate calcium signaling and nitric oxide production through polycystin-1. Circulation 2008, 117:1161-1171. 10.1161/CIRCULATIONAHA.107.710111, 3071982, 18285569.
28. Guadiana SM, Semple-Rowland S, Daroszewski D, Madorsky I, Breunig JJ, Mykytyn K, Sarkisian MR. Arborization of dendrites by developing neocortical neurons is dependent on primary cilia and type 3 adenylyl cyclase. J Neurosci 2013, 33:2626-2638. 10.1523/JNEUROSCI.2906-12.2013, 23392690.
29. Hoey DA, Downs ME, Jacobs CR. The mechanics of the primary cilium: an intricate structure with complex function. J Biomech 2012, 45:17-26. 10.1016/j.jbiomech.2011.08.008, 3242821, 21899847.
30. Rydholm S, Zwartz G, Kowalewski JM, Kamali-Zare P, Frisk T, Brismar H. Mechanical properties of primary cilia regulate the response to fluid flow. Am J Physiol Renal Physiol 2010, 298:F1096-F1102. 10.1152/ajprenal.00657.2009, 20089672.
31. Downs ME, Nguyen AM, Herzog FA. Hoey DA 2012, Jacobs CR: An experimental and computational analysis of primary cilia deflection under fluid flow. Comput Methods Biomech Biomed Engin, [Epub ahead of print.].
32. Schwartz EA, Leonard ML, Bizios R, Bowser SS. Analysis and modeling of the primary cilium bending response to fluid shear. Am J Physiol 1997, 272:F132-F138.
33. Young YN, Downs M, Jacobs CR. Dynamics of the primary cilium in shear flow. Biophys J 2012, 103:629-639. 10.1016/j.bpj.2012.07.009, 22947924.
34. Shiba D, Yamaoka Y, Hagiwara H, Takamatsu T, Hamada H, Yokoyama T. Localization of Inv in a distinctive intraciliary compartment requires the C-terminal ninein-homolog-containing region. J Cell Sci 2009, 122:44-54. 10.1242/jcs.037408, 19050042.
35. Shiba D, Manning DK, Koga H, Beier DR, Yokoyama T. Inv acts as a molecular anchor for Nphp3 and Nek8 in the proximal segment of primary cilia. Cytoskeleton (Hoboken) 2010, 67:112-119.
36. Ghossoub R, Molla-Herman A, Bastin P, Benmerah A. The ciliary pocket: a once-forgotten membrane domain at the base of cilia. Biol Cell 2011, 103:131-144. 10.1042/BC20100128, 21275905.
37. Ostrowski LE, Dutcher SK, Lo CW. Cilia and models for studying structure and function. Proc Am Thorac Soc 2011, 8:423-429. 10.1513/pats.201103-027SD, 3209580, 21926393.
38. Hart CY, Burnett JC, Redfield MM. Effects of avertin versus xylazine-ketamine anesthesia on cardiac function in normal mice. Am J Physiol Heart Circ Physiol 2001, 281:H1938-H1945.
39. Kang JJ, Toma I, Sipos A, McCulloch F, Peti-Peterdi J. Quantitative imaging of basic functions in renal (patho)physiology. Am J Physiol Renal Physiol 2006, 291:F495-F502. 10.1152/ajprenal.00521.2005, 16609147.
40. Ditlevsen S, Yip KP, Holstein-Rathlou NH. Parameter estimation in a stochastic model of the tubuloglomerular feedback mechanism in a rat nephron. Math Biosci 2005, 194:49-69. 10.1016/j.mbs.2004.12.007, 15836864.
41. Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, Kanai Y, Kido M, Hirokawa N. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 1998, 95:829-837. Erratum in: Cell 1999, 99:117, 10.1016/S0092-8674(00)81705-5, 9865700.
42. Essner JJ, Vogan KJ, Wagner MK, Tabin CJ, Yost HJ, Brueckner M. Conserved function for embryonic nodal cilia. Nature 2002, 418:37-38. 10.1038/418037a, 12097899.
43. Caspary T, Larkins CE, Anderson KV. The graded response to Sonic Hedgehog depends on cilia architecture. Dev Cell 2007, 12:767-778. 10.1016/j.devcel.2007.03.004, 17488627.
44. Fan Y, Esmail MA, Ansley SJ, Blacque OE, Boroevich K, Ross AJ, Moore SJ, Badano JL, May-Simera H, Compton DS, Green JS, Lewis RA, van Haelst MM, Parfrey PS, Baillie DL, Beales PL, Katsanis N, Davidson WS, Leroux MR. Mutations in a member of the Ras superfamily of small GTP-binding proteins causes Bardet-Biedl syndrome. Nat Genet 2004, 36:989-993. 10.1038/ng1414, 15314642.
45. Roepman R, Letteboer SJ, Arts HH, van Beersum SE, Lu X, Krieger E, Ferreira PA, Cremers FP. Interaction of nephrocystin-4 and RPGRIP1 is disrupted by nephronophthisis or Leber congenital amaurosis-associated mutations. Proc Natl Acad Sci U S A 2005, 102:18520-18525. 10.1073/pnas.0505774102, 1317916, 16339905.
46. Liu X, Udovichenko IP, Brown SD, Steel KP, Williams DS. Myosin VIIa participates in opsin transport through the photoreceptor cilium. J Neurosci 1999, 19:6267-6274.
47. Fliegauf M, Horvath J, von Schnakenburg C, Olbrich H, Müller D, Thumfart J, Schermer B, Pazour GJ, Neumann HP, Zentgraf H, Benzing T, Omran H. Nephrocystin specifically localizes to the transition zone of renal and respiratory cilia and photoreceptor connecting cilia. J Am Soc Nephrol 2006, 17:2424-2433. 10.1681/ASN.2005121351, 16885411.
48. Berbari NF, Pasek RC, Malarkey EB, Yazdi SM, McNair AD, Lewis WR, Nagy TR, Kesterson RA, Yoder BK. Leptin resistance is a secondary consequence of the obesity in ciliopathy mutant mice. Proc Natl Acad Sci U S A 2013, 110:7796-7801. 10.1073/pnas.1210192110, 23599282.
49. Hebrok M, Kim SK, St Jacques B, McMahon AP, Melton DA. Regulation of pancreas development by hedgehog signaling. Development 2000, 127:4905-4913.
50. Zhang Q, Davenport JR, Croyle MJ, Haycraft CJ, Yoder BK. Disruption of IFT results in both exocrine and endocrine abnormalities in the pancreas of Tg737(orpk) mutant mice. Lab Invest 2005, 85:45-64. 10.1038/labinvest.3700207, 15580285.
51. Kunimoto K, Yamazaki Y, Nishida T, Shinohara K, Ishikawa H, Hasegawa T, Okanoue T, Hamada H, Noda T, Tamura A, Tsukita S, Tsukita S. Coordinated ciliary beating requires Odf2-mediated polarization of basal bodies via basal feet. Cell 2012, 148:189-200. 10.1016/j.cell.2011.10.052, 22265411.
52. Nishimura Y, Kurisaki A, Nakanishi M, Ohnuma K, Ninomiya N, Komazaki S, Ishiura S, Asashima M. Inhibitory Smad proteins promote the differentiation of mouse embryonic stem cells into ependymal-like ciliated cells. Biochem Biophys Res Commun 2010, 401:1-6. 10.1016/j.bbrc.2010.08.099, 20807502.